Mammalia, Chiroptera, Phyllostomidae, Lonchophylla Hesperia G

n Mammalia, Chiroptera, Phyllostomidae, Lonchophylla hesperia G. M. Allen, 1908: Second record of the Western

istributio Nectar Bat in Ecuador after 70 years D

1* 2 1,2 3 raphic Diego G. Tirira , Santiago F. Burneo , Carlos E. Boada and Simón E. Lobos g

eo 1 Fundación Mamíferos y Conservación, Víctor Balseca 100. Conocoto, Quito, Ecuador. G n o

2 EPontificiacuador. Universidad Católica del Ecuador, Museo de Zoología. Avenida 12 de Octubre 1076 y Roca. Quito, Ecuador. * 3 CorrPontificiaesponding Universidad author. CatólicaE-mail: [email protected] Ecuador, Centro de Investigación en Enfermedades Infecciosas. Avenida 12 de Octubre 1076 y Roca. Quito, otes N Abstract: Herein we report the second record for Lonchophylla hesperia captured an adult male in a mountainous dry valley at Comunidad San Jacinto, Catamayo Valley, Loja Province, southwestern in Ecuador, and the first one since 1939. We

areEcuador. presented, The dominant indicating landscape the areas consists between of the agricultural two countries lands, were mainly the ofhabitat corn fieldsis climatically and pastures; suitable while for theits presence.natural forest is restricted to small patches. A description of the species’ shelter and a predictive distribution model in Peru and Ecuador

The genus Lonchophylla is specialized on a diet of unpublished and unknown for 50 years. Consequently, this nectar and pollen; therefore they are known as Nectar species has been traditionally treated as endemic to Peru Bats (Wilson and Cole 2000). As part of this adaptation, (e.g. they have a much longer snout and tongue than any other 2008); an endemism not mentioned by Koopman (1993), bats, except other genera of glossophagines, such as Simmons Nowak (2005) 1994; and Pacheco Pacheco 2002; et al. (2009). Griffiths and Gardner Platalina Thomas, 1928; and Musonycteris Schaldach and McLaughlin, 1960 2008). The genus is characterized by a tongue with a deep lateral groove and (Nowak without 1994;hair-like Griffiths papillae and on Gardner tip; the central upper incisors are long, larger than lateral ones; and wings terminate at base of ankles (Nowak 1994; Tirira upper premolars differ, the first shorter than the second; The genus is endemic to the Neotropics, with a wide distribution2007; Griffiths in and rainforests Gardner from2008). Nicaragua south to the Guianas, Bolivia and southeastern Brazil. Moreover, this is one of the most diverse genera of bats in the Neotropics, with 12 species (Woodman 2007). Nine of these are found in Ecuador (Tirira 2007; Woodman 2007; Mantilla-Meluk et al. 2009), mainly in tropical evergreen rainforest and subtropical forest, in northwestern and Amazonia. Only L. hesperia is found in the southwestern dry forest (Tirira 2007). Lonchophylla hesperia G. M. Allen, 1908, the Western Nectar Bat, is restricted to northwestern Peru (Pacheco

Ecuador (Albuja 1991; Tirira 1999). In Peru the species 2002; Griffiths and Gardner 2008), and southwestern arid marginal portion of the Amazon drainage (Koopman 1978).is known In to Ecuador, occur from the the species tropical is knownarid Pacific only coast from to one an

1,600 m), approximately 30 km south of the city of Loja, in Lojarecord Province confirmed (Albuja from 1999; Malacatos Tirira 2007) (04°18’ (Figure S, 79°16’ 1). This W, specimen was collected on 23 August 1939, by L. Gómez, Figure 1. Distribution of the Western Nectar Bat (Lonchophylla hesperia). and is deposited at the Field Museum of Natural History of Chicago (FMNH 53536) (FMNH data base). This species Gardner (2008). Dark blue shading represents the predictive distribution modelBlack lines in Ecuador represent and the Peru. current Yellow distribution dots represent as reported the previous by Griffiths known and

Albuja (1991), yet the record from Malacatos remained reported in this work (Comunidad San Jacinto, Loja province). was mentioned for first time to the Ecuadorian fauna by Ecuadorian and Peruvian localities. Red dot represents the new locality

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The Ecuadorian locality of Malacatos is in subtropical No information about use of man-made shelters has dry forest, known as Matorral Seco Montano (according to been previously mentioned. This specimen was found in an old inhabited house that demonstrates the species by an annual rainfall from 390 to 590 mm and an annual may be found in association with human buildings. The the classification of Sierra 1999), which is characterized occurrence of this species in disturbed areas may indicate the Southwestern Subtropical Ecuadorian zone (Albuja et some tolerance to localities that have been impacted by al.mean 1980). temperature Here we report of 23.7°C the (Sierra second 1999). record The for this area species is into human activity. The morphological measurements reported are presence in the country. within the known range for the species. Selected external in Ecuador,The Western 70 years Nectar after Bat its is first one collection, of the rarer confirming Neotropical its and cranial measurements (in mm) of the specimen bat species (Koopman 1978; Tirira 2007). Tuttle (1970) measurements reported by Allen (1908), Gardner (1976), and 1964, in which 54 species of bats to the north and SwanepoelQCAZ 10888, and followed Genoways by (1979), maximum Woodman and and minimum Timm centraldid not trap Peru this were species reported. during Pacheco field work et al. between (2007), 1963 in a (2008), are: head and body length, 59.1 (51–68); tail length, 8.7 (7–13); hindfoot bats corresponding to 35 species, but only three were length,(2006), 9.3and (8–15);Griffiths earand length,Gardner 13.9 (10–16); forearm study of five localitiesL. hesperia in. Carreranorthwestern et al. (2010), Peru, trapped conducting 377 length, 38.3 (36–40.6); thumb length, 9.4 (8.5–9); leaf- L. hesperia in a nose length, 7.5 (8); calcar length, 8.5 (8.5–9.5); caudal identifiedstudy that astrapped 1,580 bats corresponding to 66 species membrane length, 20.9 (21); tibia length, 15.3 (14–15); infield 16 work localities in 2001 in western and 2004, Ecuador did not (10 collect of those localities greatest length of skull, 27.0 (25.4–28.0); condylobasal were in the dry forest of the central and southwestern area length, 25.6 (24.5–26.1); zygomatic width, 9.7 (10.0– of the country). That level of abundance is not corroborated 10.1); braincase breadth, 8.8 (9.1–9.5); palatal length, 15.2 by Thomas and Thomas (1977), who collected eight (14.7–16); postorbital constriction, 4.7 (4.7–4.9); mastoid breath, 9.4 (9.7–10); width across canines, 4.1 (4.2–4.3); Lonchophylla hesperia. Currently, the species is known width across molars, 5.7 (5.6–5.8); length of maxillary frombats 19 in individuals three nights, corresponding four of which to nine were localities, identified six asof toothrow, 8.8 (8.3–9); mandibulary length, 19.2 (20.3); which are known from a single record (Table 1). length mandibular toothrow, 9.4 (9.4). Body weight was Altitudinal records reported for the species indicate not taken (literature: 10 g). This individual had the typical diagnostic features 1976) to 1,600 m in Malacatos (Tirira 2007). for L. hesperia according to Allen (1908), Woodman it occursOn July from 14 2008sea level we collectedin Zorritos a singleand Trujillo individual (Gardner of L. hesperia Gardner (2008), including: medium-sized to the genus (in altitude 1,258 m), Catamayo Valley, Loja Province, on the factand L. Timm hesperia (2006), is the Woodman smallest Lonchophylla (2007), and Griffithsin the group and slopes of in the Comunidad southwestern San Ecuadorian Jacinto (03°59’ Andes. S, 79°21’ As in the W, comprising the larger species of the genus; Woodman and dry forest, known as Matorral Seco Montano. San Jacinto Gardner 2008); dorsum pale brown, and venter grayish isfirst located Ecuadorian in a mountainous record, it was valley collected with smallin subtropical streams brown,Timm 2006;paler than Tirira back; 2007; and Woodman forearm shorter 2007; Griffithsthan 41 mm, and but longer than 36 mm. The thumb measurement differs of(dry human most disturbance,of the year), atmostly the confluence agricultural of zonesthe Catamayo such as who mention that thumb length is shorter than 7.0 mm. River system. The dominant landscape consists of areas However,from that inreported the collected by Griffiths specimen and thumb Gardner was (2008: longer 247), (9.4 forest. The incline of the terrain is moderately pronounced mm), as was reported by Allen (1908) (8.5 to 9.0 mm). cornwith slopes fields of and 30% pastures, or more. with small patches of natural The cranial and dental diagnostic features were also similar to those described in the literature (Allen 1908; ethanol) and cleaned and dried skull of an adult male with scrotalThe testes.specimen The consists individual of ais fluid-preserved deposited in the body Mammals (75% and Gardner 2008): skull narrow and elongated; rostrum Woodman and Timm 2006; Woodman 2007; Griffiths

DivisionThe individual of Museo was de encountered Zoología (QCAZ resting 10888)in its day at roost, the elongated and inflated; supraorbital region narrow and approximatelyPontificia Universidad 4 m above Católica the ground del Ecuador, in a small in Quito. inhabited essentiallyinflated; greatest alike in form length and of size; skull conspicuous longer than gap between 25 mm, rustic dwelling, composed of a single room without closed but shorter than 28 mm; first and second upper molars attic. The bat was captured upon being manually stricken margins of upper incisors not transcribing a smooth arc; widthouter margins across molars of first andless secondthan 6 uppermm; mastoid incisors; width outline less of than 10 mm; length of maxillary toothrow less than 9 mm. relativefrom its flight position path, in at the 16:00 dwelling: h. Three Desmodus other bat species rotundus were (E. Some cranial measurements of the specimen were identifiedGeoffroy St.-Hilare,in the same 1810), shelter, Glossophaga but without soricina an apparently (Pallas, somewhat smaller (zygomatic width, braincase breadth, 1766), and Artibeus fraterculus Anthony, 1924. The bat mastoid breath, width across canines) than those reported colony included approximately 100 individuals, where the in the literature. However, the maximum and minimum dominant species was Desmodus rotundus (comprising measurements for the species were based on few records 80% or more of the mixed-species group). Only a few (sometimes only one or two), therefore we did not consider specimens of G. soricina and A. fraterculus were observed; this variation to be relevant. no additional individuals of L. hesperia were registered. Most of the conservation status of L. hesperia remains

Check List | Volume 7 | Issue 3 | 2011 316 Tirira et al. | Second record of Lonchophylla hesperia in Ecuador after 70 years unknown. It is believed to be threatened by the intense based on scarce and widely separated points (Hernandez clearing of dry forests that has been taking place in et al. 2006). If such run were not part of the analysis the southwestern Ecuador and northwestern Peru, which has diminished the extent of its natural habitat considerably theAUC distribution would have patternbeen of of0.912 the (SDspecies. = 0.118), which gives us confidenceThe model in using was the generated model as in a logistictool for understanding output format 2008),(Tirira 2011).and then According downlisted to the to IUCNNear RedThreatened List, the in species 2009 and the presence/absence threshold used was 0.157, was first assessed as Vulnerable (evaluated in 1996 and decline(Solari and (but Velazco probably 2009). at a The rate current of less categorythan 30% is overjustified ten calculationswhere both coincided. “Equal Training Sensitivity and Specificity” years).due to This the factdecline that is thea result species of widespread is likely in habitat significant loss andThe “Maximum model predicts Training the distribution Sensitivity of plus the Specificity”L. hesperia and degradation throughout much of its range, which by habitat suitability in areas where the species has not makes the species close to qualifying for Vulnerable (Solari yet been observed (Figure 1), including Peruvian and and Velazco 2009). Ecuadorian Amazonia that may not be part of the realized niche, likely due to interactions with other species or Mammals of Ecuador In (TiriraEcuador 2001), the species but was was changed classified to historical factors such as geographic barriers limiting Endangeredas Vulnerable in inthe the second first edition (Tirira of the 2011). Red Book In Peru, of the it dispersion rather than climatic conditions. is treated as Vulnerable (Decreto Supremo No. 034-2004- The climatic aspects of the fundamental niche predicted AG in Pacheco et al. 2009). The species is expected to occur by the model includes an annual mean temperature of

Cerrosin some de protected Amotape areas, National like Arenillas Park and Ecological Tumbes NationalReserve this21.1°C species (±3.54), has been and arecorded, low mean Malacatos annual precipitationand San Jacinto, of and Puyango Petrified Protected Forest (in Ecuador), and 602 mm (±535). The two Ecuadorian localities in which Our new record of Lonchophylla hesperia was combined respectively. Also, two bioclimatic variables explained 83% Reservewith the (in eight Peru). other records (Table 1) to generate a ofcorrespond the variation to 20.1°Cseen in /the 789 model: mm the and annual 21.4°C precipitation / 790 mm, predictive distribution model using a Maximum Entropy (responsible for 48.1% of the variation), and precipitation approach implemented in Maxent software package during the warmest quarter (model average: 59.1 mm). (Phillips et al. 2006). Nineteen bioclimatic variables, at 30 These values suggest an adaptation to dry weather and second per pixel resolution, were used as environmental drought tolerance for the species. variables (from WorldClim, Hijmans et al. 2005). Eight An interesting result of the modeling is that suitable replications of the model were run using jackknife with areas for the species does not only include dry warm one record in each run (Pearson et al. 2007), and model regions (such as in the Ecuadorian records) or dry coastal performance was evaluated by measuring the area under forests, but also dry areas of higher altitude where the

This methodology has been proven useful for species with Cotopaxi Province at 3,000 m above sea level, or as low as smallthe Receiver numbers Operating of occurrence Characteristic records (Brotons (ROC) curve et al. (AUC). 2004; mean temperature could be as low as 12°C, such as Allouche et al. 2006; Elith et al. in these locations is still relatively low (675 and 883 for the model replications were 0.810 (minimum = 0.298, mm,10°C at respectively). 3,300 m in Cañar Within Province. suitable Annual areas predictedprecipitation by maximum = 0.997; SD = 0.272). The 2006). high standard The average deviation AUC the distribution model, the highest annual precipitation is caused by one of the repetitions that failed to predict the occurs in small patches in northwestern Ecuador, in Esmeraldas Province, where annual rainfall reaches 1,300 one run. This is a common effect in distribution models mm. southernmost Peruvian point, lowering the AUC for that Table 1. Lonchophylla hesperia), in chronological order.

DEPARTMENT Records of / the Western Nectar Bat ( LOCALITY ALTITUDE SPECIMENS REPORTED SOURCE PROVINCE Peru 6 Tumbes 0 Allen (1908) (counting the holotype and two paratypes) La Libertad TrujilloZorritos 0 1 Tuttle (1970), Gardner (1976) Cajamarca Jaén 740 1 Gardner (1976) Tumbes 5 km E Puerto Pizarro 5 4 Thomas and Thomas (1977) Amazonas Bagua Grande 724 1 Koopman (1978) Piura Piura 27 1 Koopman (1978) Tumbes Angostura 74 3 Pacheco et al. (2007) Ecuador Loja Malacatos 1,600 1 Albuja (1991) Loja San Jacinto 1,258 1 This publication

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As information on the natural history of this species accumulates, analyses should be made to assess resource Chiroptera, Phyllostomidae, Lonchophylla pattoni Mantilla-Meluk,Ecuador. Investigación, H., A.M. Jiménez-Ortega Biodiversidad and y Desarrollo R.J. Baker. 28(2): 2009. 222-225. Mammalia, availability in predicted areas, since the model does not Walker’s Bats of the World. Baltimore:: first record The Johns for feeds on. Meanwhile, caution should be taken when Nowak,Pacheco, R.M. V. 2002. 1994. Mamíferos del Perú; p. 503-549. In G. Ceballos and J.A.Hopkins Simonetti University (ed.). Press. Diversidad 287 p. y conservación de los mamíferos interpretingtake into account the resulting the abundance distribution of flowers model; this it species should neotropicales be considered a tool to direct future collecting efforts Autónoma de México. . México, DF: CONABIO and Universidad Nacional occupancy limits of the species. Pacheco,and adjacent V., R. Cadenillas, dry forest S.in northwestern Velazco, E. Salas Peru. and Acta U. Chiropterologica Fajardo. 2007. and to gather information that would further refine the 9(2):Noteworthy 409-422. bat records from the Pacific Tropical rainforest region Acknowledgments: This specimen was collected under Permit No. Diversidad y endemismo de los mamíferos del Perú. Revista Peruana Ecuador. The collection was part of the Chagas Disease Project (directed Pacheco,de Biología V., R. 16(1): Cadenillas, 5-32. E. Salas, C. Tello and H. Zeballos. 2009. by016-07 Mario IC-FAU-DNBAPVS/MA J. Grijalva), that was carriedissued outby the by theMinisterio Centro dedel Investigación Ambiente of en Enfermedades Infecciosas and Servicio Nacional de Control de Predicting species distributions from small numbers of occurrence Enfermedades Transmitidas por Vectores Artrópodos. This project was Pearson,records: R.G., a C.J.test Raxworthy, case using cryptic M. Nakamura geckos inand Madagascar. A.T. Peterson. Journal 2007. of supported by the Division of Microbiology and Infectious Diseases, Biogeography 34: 102-117. National Institute of Allergy and Infectious Diseases, and National modeling of species geographic distributions. Ecological Modelling Phillips,190(3-4): S.J., R.P. 231-259. Anderson and R.E. Schapire. 2006. Maximum entropy Institutes of Health of the USA, UNICEF/UNPD/World Bank/WHO Special Propuesta preliminar de un sistema de clasificación deProgram Salud Pública for Research del Ecuador. and Training Also, we in wish Tropical to express Diseases our (TDR/WHO), gratitude to de vegetación para el Ecuador continental. Quito: Proyecto INEFAN- PLAN International Ecuador, Children’s HeartLink, USA; and Ministerio Sierra, R. (ed.). 1999. Simmons, N.B. 2005. Order Chiroptera; p. 312-529. In D.E. Wilson and the Museo de Zoología at the Pontificia Universidad Católica del Ecuador GEF-BIRF and EcoCiencia.Mammal 194 Species p. of the World, a Taxonomic and Swing,(QCAZ), Mariana for allowing M. Vale, us and to an review anonymous and measure reviser thefor their specimen, comments and to Geographic Reference. 3rd edition. Baltimore: The Johns Hopkins theBrian manuscript. S. Arbogast, Thomas E. Lee, Jr., Mika R. Peck, C. Miguel Pinto, Kelly D.M. Reeder (ed.). Solari, S. and P. Velazco. 2009. Lonchophylla hesperia. In IUCN Literature Cited UniversityRed List of Press.Threatened Species. Version 2010.4. Electronic Database Albuja, L. 1991. Lista de vertebrados del Ecuador: mamíferos. Politécnica accessible at http://www.iucnredlist.org/. Captured IUCN on 2010. 03 March 16(3): 163-203. 2011. Albuja, L. 1999. Murciélagos del Ecuador. 2nd edition. Quito: Centro de Swanepoel, P. and H.H. Genoways. 1979. Morphometrics; p. 13-106. In Biology of Bats of the Estudio preliminar New World Family Phyllostomatidae (Part III). Lubbock: Special deZoología los vertebrados de Vertebrados, ecuatorianos. Escuela Quito: Politécnica Editorial Nacional. Escuela 288 Politécnica p. R.J. Baker, J.K. Jones Jr. and D.C. Carter (ed.). Albuja,Nacional. L., M. Ibarra,143 p. J. Urgilés and R. Barriga. 1980. Allen, G.M. 1908. Notes on Chiroptera. Bulletin of the Museum of fromPublications Northern of Peru.the Museum Biotropica of Texas 9(2): Tech131-132. University 16: 1-441. Comparative Zoology 52(3): 25-63. Tirira,Thomas, D.G. R. and (ed.). K.R. 1999. Thomas. Mamíferos 1977. A delsmall-vertebrate Ecuador. 1st Thanatocenosis edition. Quito:

species distribution models: prevalence, kappa and the true skill SIMBIOE. Publicación Especial sobre los mamíferos del Ecuador 2. Allouche,statistic O., (TSS). A. Tsoar Journal and of R. Applied Kadmon. Ecology 2006. 43(6): Assessing 1223-1232. the accuracy of 392Museo p. de Zoología, Pontificia Universidad Católica del Ecuador and Brotons, L., W. Thuiller, M.B. Araújo and A.H. Hirzel. 2004. Presence- Tirira, D.G. (ed.). 2001. Libro Rojo de los mamíferos del Ecuador. 1st absence versus presence-only modelling methods for predicting bird edition. Quito: SIMBIOE, EcoCiencia, Ministerio del Ambiente and habitat suitability. Ecography 27(4): 437-448. Carrera, J.P., S. Solari, P.A. Larsen, D.F. Alvarado-Serrano, A.D. Brown, C. los mamíferos del Ecuador 4. 236 p. Tirira,IUCN. D.G. Serie 2007. Libros Guía Rojos de campo del Ecuador de los mamíferos 1. Publicación del Ecuador. Especial Quito:sobre of Western Ecuador. Special Publications, Museum of Texas Tech Ediciones Murciélago Blanco. Publicación Especial sobre los CarriónUniversity B., 57: J.S. 1-37.Tello and R.J. Baker. 2010. Bats of the tropical lowlands mamíferos del Ecuador 6. 576 p. Tirira, D.G. (ed.). 2011. Libro Rojo de los mamíferos del Ecuador. 2nd

Elith, J., C.H. Graham, R.P. Anderson, M. Dudík, S. Ferrier, A. Guisan, R.J. occurrenceHijmans, F. data. Huettmann, Ecography J.R. 29(2): Leathwick 129-151. and A. Lehmann. 2006. Ecuador.edition. Quito: Publicación Fundación Especial Mamíferos sobre los y mamíferos Conservación, del Ecuador Pontificia 8. Gardner,Novel A.L. methods 1976. The improve distributional prediction status of of species’ some Peruvian distributions mammals. from 400Universidad p. Católica del Ecuador y Ministerio del Ambiente del Occasional Papers of the Museum of Zoology, Louisiana State University Tuttle, M.D. 1970. Distribution and zoogeography of Peruvian bats, 42: 1-18. with comments on natural history. The University of Kansas Science Bulletin 49(2): 45-86. In A.L. Gardner (ed.). Mammals of South Common Names of Mammals of the World. Griffiths,America. T.A. and Volume A.L. Gardner. 1: Marsupials, 2008 [2007]. Xenarthrans, Subfamily Shrews, Lonchophyllinae and Bats. Washington, DC: Smithsonian Institution. 204 p. Griffiths, 1982; p. 244-255. Woodman,Wilson, D.E. and N. 2007.F.R. Cole. A 2000. new species of nectar-feeding bat, genus Hernandez, P.A., C.H. Graham, L.L. Master and D.L. Albert. 2006. The Lonchophylla, from western Colombia and western Ecuador effectChicago of andsample London: size andThe Universityspecies characteristics of Chicago Press. on performance of (Mammalia: Chiroptera: Phyllostomidae). Proceedings of the different species distribution modeling methods. Ecography 29(5): Biological Society of Washington 120(3): 340-358. 773-785. relationships of nectar-feeding bats, with descriptions of new high resolution interpolated climate surfaces for global land areas. Woodman,Lonchophylla N. and from R.M. western Timm. South 2006. America Characters (Mammalia: and phylogenetic Chiroptera: Hijmans,International R.J., S.E. Cameron,Journal of J.L.Climatology Parra, P.G. 25(15): Jones and1965-1978. A. Jarvis. 2005. Very Phyllostomidae: Lonchophyllini). Proceedings of the Biological Society of Washington 119(4): 437-476. emphasis on the role of the Andes. American Museum Novitates 2651: Koopman,1-33. K.F. 1978. Zoogeography of Peruvian Bats with special : January 2011 Koopman, K.F. 1993. Order Chiroptera; p. 137-241. In D.E. Wilson and : March 2011 Mammal Species of the World, a Taxonomic and Received : March 2011 Geographic Reference. 2nd edition. Washington, DC: Smithsonian Last Revised : May 2011 InstitutionD.M. Reeder Press (ed.). and American Society of Mammalogists. Accepted Published online Editorial responsibility: Marcelo R. Nogueira

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