New records of bats from the northern region of the Peruvian Amazon

M Mónica Díaz

[PIDBA (Program of Argentine Biodiversity Research), Faculty of Natural Science and Institute Miguel Lillo, National University of Tucuman-PCMA (Program of Argentine Bat Conservation) CONICET (National Council of Scientific and Technical Research), Miguel Lillo 205, CP. 4000, Tucumán, Argentina]

New records of bats from the northern region of the Peruvian Amazon

M Mónica Díaz*

[PIDBA (Program of Argentine Biodiversity Research), Faculty of Natural Science and Institute Miguel Lillo, National University of Tucuman-PCMA (Program of Argentine Bat Conservation) CONICET (National Council of Scientific and Technical Research), Miguel Lillo 205, CP. 4000, Tucumán, Argentina]

The northern Amazon Basin in Peru is one of the most diverse areas for small mammals in the world. In this work, I present information related to the diversity of bat species in the Amazonian region of Iquitos, Peru, where nearly 60% of the 152 bat species known to Peru recorded. Unlike in previous investigations in this area, bat surveys were designed to detect species living in urban and rural areas. The results have added a new bat species (Eumops delticus) to the Peruvian fauna, eight new species for the region around Iquitos (Peropteryx macrotis,Peropteryx pallidoptera,Anoura caudifer,Lionycteris spurrelli,Vampyrum spectrum,Thyroptera lavali,Cynomops planirostris, andMolossus coibensis), and a new species for Northeast Peru (Eumops maurus).

Chiroptera; Iquitos; Amazon; Checklist

The Amazon Basin covers millions of square kilometers and is characterized by a gradient of increasing diversity from east to west (Emmons, 1984; Voss & Emmons, 1996). The great species richness of the Peruvian Amazon is mainly due to the high heterogeneity that results from a combination of environmental factors, edaphic and ecological conditions, and historical processes (Gentry, 1986; Salo et al, 1986; Kalliola et al, 1993; Tuomisto et al, 1995; Alvarez Alonso, 2002).

Iquitos is a region known worldwide for its high diversity of wildlife species (Gentry, 1988; Rodríguez & Duellman, 1994; Lamar, 1997; Díaz & Willig, 2004), including a high diversity of small mammals (Hice, 2003; Hice et al, 2004). Approximately 60% of the 152 species of bats in Peru can be found in this region around Iquitos (Pacheco, 2002). As a result of the intensive surveys conducted in this area, several new records of small mammal species have been added to the Iquitos region (Hice & Solari, 2002; Hice, 2003; Angulo & Díaz, 2004; Díaz & Willig, 2004; Hice et al, 2004). The studies of Hice et al (2004) carried out at the Reserva Nacional de Allpahuayo Mishana (25 km west of Iquitos) recorded 65 species of bats that made that area as the second richest area for bats species in Peru, after Parque Nacional de Manu. For other areas located in the Department of Loreto, 63 (Ascorra et al, 1993; Solari et al, 1999) and 57 species of bats (Fleck et al, 2002) were recorded.However, those surveys conducted in specific areas focused mainly on natural environments with variable degrees of human impact; they did not include suburban and urban areas. Thus, knowledge about bats of these urban environments was available only from specimens collected occasionally or found accidentally in towns (Avila-Flores & Fenton, 2005). Although the urbanization processes may have harmful effects on bats, leading to dramatic declines in diversity and abundance (Avila-Flores & Fenton, 2005; Oprea et al, 2009), it should be noted that they also provide shelter as well as food. Some species benefit from the concentrations of insects clustered around streetlights (Fenton, 1997; Everette et al, 2001). For these reasons, I decided to intensify collection efforts in urban and suburban areas, resulting in the inclusion of several species new to this area, as well as several new species for Peru.

1 Materials and Methods

The species reported here were collected from December 2002 to December 2006, at 14 collecting sites along the Iquitos-Nauta Highway (see Appendix I, Fig. 1), which passes through several districts of the Province of Maynas, Loreto Department. The overall study area is located in the “Iquitos region” (as referred to by Ortiz-S, 1997) and includes the northeastern Amazon Basin of Peru, and the adjacent part of southern Colombia. The region is dissected by several rivers and streams, and the elevation ranges from 100 to 220 m, with low-lying areas characterized by flooded forests (igapo) and higher areas supporting white sand forests (varillal) and upland forests (monte alto) (Ruokolainen & Tuomisto. 1993; Willig et al, 2007). The climate is relatively uniform, warm (average annual temperatures between 25 - 27°C), humid (annual mean humidity 85%), and rainy (annual mean precipitation 2700 mm) (Encarnación, 1985; Tafur Rengifo, 2001).

Fig. 1 Map of localities for collected bats (see details of localities in the Appendix I).

The study sites included primary and secondary forests, as well as rural, suburban, and urban areas. All bats were captured with mist nets placed at different heights, from the ground up to the sub-canopy and canopy levels. Nets were set from 18:00 h until 01:00 h and were checked every hour. Some specimens were collected by searching diurnal roosts in tree cavities, foliage, culverts, and buildings, among other places.

Total capture effort was 60,552 net-meter-hours, and the capture effort by habitat was 13,806 net-meterhours for primary forest, 16,890 for secondary forest, 12,648 for urban areas, 12,900 for rural areas, 1,812 for suburban areas, 720 for primary-secondary forest ecotones and 1,776 for secondary forest-rural area ecotones. A total of 5,510 specimens were captured, from which 3,436 were collected and 2,089 released. Of the total, 5,270 were captured in mist nets and 255 were captured in roosts.

External measurements, body mass, sex, and reproductive condition were recorded in the field for all specimens, following Díaz et al (1998). Voucher specimens were prepared as skins and skeletons or stored in alcohol. The specimens are still being catalogued. A portion of the specimens will be deposited at the Museo de Historia Natural, Universidad Nacional Mayor de San Marcos (UNMSM), Lima, Peru, and another portion will be deposited at the Colección Mamíferos Lillo (CML), Tucumán, Argentina. The acronyms used in the text are MMD (personal catalogue of María Mónica Díaz) and CML (Colección Mamíferos Lillo).

The external measurements were taken from fresh specimens using a ruler, and forearm and cranial measurements were taken with a digital caliper to the nearest 0.05 mm. All measurements were taken as described by Barquez et al (1999), but I add the condyleincisive length, measured as the distance from the anteriormost plane of the upper incisors back to the posteriormost projection of the occipital condyles. The measurements and their abbreviations are as follows: total length (ToL), tail length (TL), hindfoot length (HFL), ear length (EL), forearm length (FA), weight (W), body mass in grams, greatest length of skull (GLS), condyle-incisive length (CIL), breadth of braincase (BB), least interorbital breadth (LIB), postorbital constriction (PC), zygomatic breadth (ZB), mastoidal breadth (MB), palatal length (PL), length of maxillary toothrow (LMxT), width across upper canines (C-C), width across upper molars (M-M), length of mandible (LM), and length of mandibular toothrow (LMdT).

The Specimens Examined indicates the amount of individuals collected per locality, their sex and their catalogue numbers. Additional Records are given for some species when they were registered in a nearby locality. Under Remarks, some general comments are added, mainly related to field, systematic, or distributional observations, as well as activity and habitat. The new records are explained in the species accounts.

2 Results

The intensive mist-netting and searching for bats in roosts, conducted over nearly five years, has allowed for the extension of the previously known distributions for ten species (families Emballonuridae, Phyllostomidae, and Molossidae), including nine species new to the region and one new species for Peru. For each species, the general distribution is mentioned.

SPECIES ACCOUNTS

ORDER CHIROPTERA

Family Emballonuridae Gervais, 1855

Peropteryx macrotis (Wagner, 1843)

Distribution This species has a wide distribution from southern Mexico south to Bolivia and Paraguay (Hood & Gardner, 2007).

Specimens Examined (1) IQUITOS: Iquitos, Edificio EsSalud (calles Raymondi-Napo), 1 female (MMD 4875).

Additional Records Puerto Indiana, Amazon River (not examined), collected in 1926 by Olalla and sons, and deposited at the American Museum of Natural History (AMNH), New York.

Remarks The only specimen was collected in downtown Iquitos near dusk, at 6:00 pm on the 5th of July 2005, in a mist net placed in the 10th floor of a building. It was a pregnant female with a fetus of Crown Rump (CR) length of 12 mm. In the same building, several specimens ofMyotis albescensandMolossus coibensiswere collected.

This species is distributed throughout the Peruvian Amazon. Although previously there were no specimens cited from the town of Iquitos, its presence was probable, as mentioned by Hice et al (2004) for the Reserva Nacional Allpahuayo-Mishana.

The measurements of the specimen from Iquitos (Tab. 1) are in the upper limits for the species, compared with the measurements given by Sanborn (1937), Goodwin & Greenhall (1961), and Willig (1983).

Peropteryx pallidoptera Lim et al, 2010

Distribution This species was recently described by Lim et al (2010) and was known only from three localities in Ecuador and Peru.

Specimens Examined (5) SAN JUAN: Camino a El Paujil, 1.8 km al W del km 35 de la carretera Iquitos-Nauta, 5 females (MMD 3530, 3531, 3532, 3533, 3534).

Remarks This species was found in primary lowland forests and all the specimens from Peru, cited by Lim et al (2010), were captured in their roosts. They were long ago deposited in collections; the one from Orosa was collected in 1926 by the Olalla brothers and was deposited at the AMNH. The 17 specimens from the second locality in Peru (Río Gálvez) were collected in 1998 and 1999, and later deposited at AMNH and at the MHNSM, Lima, Peru, evidencing the similarity of this species with the other “transparent wingsPeropteryx” (P. leucoptera).

The specimens indicated here in “Specimens Examined” were also collected during the day in their roosts on the 13th of July 2004 in a primary forest (but close to a deforested area). This new record represents the third locality for the distribution of the species in Peru and is located about 160 km equidistant from the other two localities. All of the specimens were females and there were four adults and one juvenile. The adults had large mammae and two of them were pregnant, one with two fetuses (CR = 7 mm) and the other with a single embryo (CR = 7 mm). Females generally give birth to a single offspring (Yee, 2000).

The roost was a large cavity on the ground, transversed by many roots of several trees, and was probably excavated by the effects of water (e.g., erosion; Fig. 2). The roost was shared with a male specimen ofCarollia brevicauda.

The most outstanding characters ofP.pallidopteraare their pale wings (Fig. 3), separated ears, and the first small peg-like upper premolar; the species can be distinguished fromP. leucopteraby the ears connected by a band, fromP. macrotisby the color of the wings, and from these two by the first upper molar, which is larger and with an accessory cusp.

Tab. 1 External and cranial measurements (acronyms are explained in Materials and Methods). The measurements, or ranges for each measurement, are shown, and then the number of specimens examined (in parentheses) is indicated

Fig. 2 Roost of Peropteryx pallidoptera; the arrow points to one of the specimens

Fig. 3 Individual of Peropteryx pallidoptera collected at the locality “Camino a El Paujil, 1.8 km al W del km 35 de la carretera Iquitos-Nauta (San Juan)”. Photo M. M. Díaz.

Family Phyllostomidae Gray, 1825

Subfamily Glossophaginae Bonaparte, 1845

Anoura caudifer (é. Geoffroy Saint-Hilaire, 1818)

DistributionAnoura caudiferis distributed throughout South America in Colombia, Venezuela, Guyana, Surinam, French Guiana, Brazil, Ecuador, Peru, Bolivia, Paraguay, and northern Argentina; its distribution forms a large arc surrounding the central Amazon Basin (Griffiths & Gardner, 2007a).

Specimens Examined (1) SAN JUAN: El Dorado, km 25 de la carretera Iquitos-Nauta, app. 1.5 km al E, 1 male (CML 7557).

Additional records Six specimens from Quebrada Orán, ca. 5 km N Río Amazonas, 85 km NE Iquitos, collected in 1984, are deposited in the Louisiana Museum of Natural History, United States of America. The specimen from San Juan represents the nearest locality to the town of Iquitos, where the species was collected.

Remarks After three years of intensive surveys, only one specimen was captured (in an ecotone between secondary forest and a deforested area) indicating that the abundance of this species is very low in the region. The specimen was an adult male, captured on July 14th 2003 at 10:00 PM during a full moon. At the same mist net, but early in the evening (before moonrise),Saccopteryx lepturaandArtibeus(Dermanura)gnomuswere also captured. The specimen ofAnoura caudiferfrom San Juan is compared here with the recently described speciesA. cadenoi, andA. aequatorisbecause of the similarity between them. The presence of a tail, and the upper canines without longitudinal sulcus, separateA. caudiferfromA. cadenoi. If compared withA. aequatoris, the uropatagium is less furred (see fig. 4b in Mantilla-Meluk & Baker, 2006). The measurements of this specimen (Tab. 1) match perfectly with those recorded by Mantilla-Meluk & Baker (2006) forA.caudifer, except for the foot, perhaps reflecting different ways to take the measure.

Subfamily Lonchophyllinae Griffiths, 1982

Lionycteris spurrelli Thomas, 1913

Distribution This species is known from eastern Panama into central Peru and northern Brazil (Griffiths & Gardner, 2007b).

Specimens Examined (1) SAN JUAN: app. 500 m E km 28.8 de la carretera Iquitos-Nauta, 1 male (MMD 4560).

Remarks from central and southeastern Peru, in Huanuco, Pasco and Cusco departments (Griffiths & Gardner, 2007b). It is here added to the Loreto Department in northeastern Peru. This species is similar to the sympatricLonchophyllathomasi, butLionycterishas a shorter rostrum than any species ofLonchophylla; it is even shorter than the braincase. InLionycteris, the upper third and fourth premolars are short and triangular, while the lower third and fourth premolars are trident with the main cusp high and robust (Woodman & Timm, 2006; Griffiths & Gardner, 2007b). The measurements of this specimen coincide with those given by Woodman & Timm (2006). This species was previously known

Fig. 4 Individual of Eumops maurus collected at the locality“Asociación de Viviendas 15 de Mayo (San Juan)”. Photo M. M. Díaz.

The only specimen was collected on April 13th 2005 at 10:00 pm, in a mist net set at ground level in primary forest. Other species collected in the same locality wereArtibeus obscurus,Carollia brevicauda,C. perspicillata,Carolliasp. (“castaneagroup”),Mesophylla macconnelli,Rhynophylla fisherae,R. pumilio,Sturnira lilium,S.tildae,Vampyressa thyone, andMyotis riparius.

Subfamily Phyllostominae Gray, 1825

Vampyrum spectrum (Linnaeus, 1758)

Distribution This species is distributed from Mexico to South America, where it is found in Colombia, Venezuela, Trinidad, Surinam, French Guiana, Ecuador, Brazil, Peru, and Bolivia (Williams & Genoways, 2007).

Specimens Examined (2) SAN JUAN: 1 km E km 25.3 de la carretera Iquitos-Nauta (Fundo San Martín), 1 female (CML 7558); km 25 de la carretera Iquitos-Nauta (Fundo San Martín), 1 female (MMD 5137).

Remarks The two specimens were collected in secondary forest habitat, on May 25th and December 11th 2006; both were adult females with closed vaginas. Twenty-six other species of bats (Emballonuridae, Phyllostomidae, and Vespertilionidae) were collected in the same area. The nearest locality where this species has been previously collected (with voucher specimens) is at Yarinacocha (Ucayali), more than 500 km SW of Iquitos, as cited by Sanborn (1949). Recently Klingbeil & Willig (2009) have mentioned the presence of this species in their study area in southwestern Iquitos, but no voucher specimens, nor a specific locality, were indicated by the authors.

Family Thyropteridae Miller, 1907

Thyroptera lavali Pine, 1993

Distribution This species has been recorded in Peru, Brazil, Ecuador, and Venezuela (Wilson, 2007). Specimens Examined (1) SAN JUAN: Zungarococha, 5.4 km al W del km 6 de la carretera Iquitos-Nauta, 1 female (MMD 716).

Remarks The only captured specimen represents the first report of the species for Iquitos, and the northernmost record for Peru. The closest known records are the type locality (Quebrada Esperanza, near the Brazilian border) (Pine, 1993) and Jenaro Herrera (Ascorra et al, 1993) (but cited asT.disciferaand later re-identified asT.lavaliby Solari et al, 2004). Both the characters and the measurements of this specimen correspond with the original description of the species (see Pine, 1993), except for the ear length, which is given as 8 mm in Pine (1993) but is 14 mm in this study. However, Reid et al (2000) indicates a range of 11-13 mm forT.lavali. The specimen from Iquitos was an adult female with a closed vagina. It was collected on December 18th 2002, at 7:00 pm, on a clear and cloudless night with a full moon, in a ground level mist net placed in secondary forest, together withCarollia perspicillata,Lophostoma silvicolum, andArtibeus(Dermanura)anderseni.

Family Molossidae Gervais, 1856

Cynomops planirostris (Peters, 1866)

Distribution This species is found east of the Andes in South America, from Colombia, Venezuela, and the Guianas, south through Peru and Bolivia, and into Paraguay and Argentina (Eger, 2007).

Specimens Examined (3) PUNCHANA: Villa del Ejército (entre Av. 28 Julio-Freyre y calle Piura), 3 females (2 MMD 5010, 5011, 1 CML 7561).

Remarks Although this species has a widespread distribution, there were previously no records for northeastern Peru. The species ofCynomopsrecorded for the area wereCynomops abrasus,C. milleri, andC.paranus(Eger, 2007).

The three specimens examined were collected in an urban area on September 20th, 2005, at 6:30 pm, during a warm and misty night with a full moon. The specimens were trapped in mist nets elevated 2 m above the ground. All were females with developed mammae; one was pregnant with a single fetus of CR=16 mm.

Eumops delticus Thomas, 1923

Distribution The distribution of this species was known from southeastern Colombia and along the Amazon River in Brazil (Eger, 2007). It is here included in Peru.

Specimens Examined (1) SAN JUAN: Piscina Olímpica del Instituto Peruano de Deportes, km 1.5 al W de la carretera Iquitos-Nauta, 1 female (CML 7560).

RemarksEumops delticuswas treated as a subspecies ofE. bonariensis(see Eger, 1977; Simmons, 2005). However Eger (2007), later decided to revalidate its specific level and restrict the distribution ofE. bonariensisto southern South America, in Brazil, Uruguay, and Argentina. During this study, only one specimen was collected in five years of surveys; this specimen represents the first record of this species for the country. The specimen was a pregnant female, with a fetus of CR=20 mm, collected at 6:30 pm on 9th October 2003. The collecting locality is close to the town of Iquitos in a recreational area. The specimen was captured in an elevated net set between a few palm trees and a swimming pool.Molossus molossuswas the only other species collected at this location.

Eumops maurus (Thomas, 1901)

Distribution This rare species is known from only a few specimens and localities (see Eger 2007) from Guyana, Surinam, Venezuela, Ecuador (Tirira, 2006; Eger, 2007), and Peru (Luna et al, 2002).

Specimens Examined (1) SAN JUAN: Asociación de Viviendas 15 de Mayo (E Av. Qui?ones), 1 female (CML 7559).

Remarks This record widely extends the distribution of this species in Peru and represents the second locality in the country. It was previously known from the Pampas del Heath, Madre de Dios (Pacheco et al, 2009), about 1000 km south of the present record. The specimen was a pregnant female with a CR=27 mm fetus, captured at 7:30 pm on July 4th, 2005, on a hot day with a clear sky, in a net elevated about 2 m above the ground. The habitat was a suburban area, with a few houses, grasses, flooded grasslands (“gramalotal”), and some yucca plants (manioc), all surrounded by secondary forests. The characters of this specimen are the typical for the species, including a band of white hairs on the ventral surface of the mesopatagium, next to body (Fig. 4). However, the forearm (55.45 mm) is slightly larger than the average for the few known specimens of this species. Other species captured at the same locality wereCarollia perspicillata,Platyrrhinusbrachycephalus, andUroderma magnirostrum.

Molossus coibensis J. A. Allen, 1904

Distribution In South America, this species is known from eastern Colombia, Peru, Ecuador, Venezuela, Guyana, French Guiana, and west-central Brazil (Eger, 2007).

Specimens Examined (15) BELEN: Moena Ca?o, 3 females (MMD 2602, 2604, 2611) and 2 males (MMD 2603, 2625). IQUITOS Colegio Primario Secundario“RADM” (Rosa Agustina Donayre de Morey), calle Putumayo, 3 females (MMD 4336, 4337, 4341) and 1 male (CML 7562); Iquitos, Edificio EsSalud (calles Raymondi-Napo), 4 females (MMD 4864, 4873, 4876, 4878). PUNCHANA: Punchana, Calle Amazonas 1086 (casa de Dr. Gendrau), 1 female (CML 7563) and 1 male (MMD 3124).

RemarksM. coibensiswas previously considered as a synonym ofM. molossusby Koopman (1993), but recently several authors (e.g., Reid et al, 2000; Simmons, 2005; Eger, 2007), following Dolan (1989), began to treat it as a valid species. Both species are similar, butM.coibensisis smaller and the dorsal pelage is shorter and practically unicolored, with a shorter white basal band of hairs and shorter and spatulated upper incisors.

Certainly, many of the specimens from Peru that are identified in the literature asMolossus molossusmay belong to this species. It is therefore essential to review these specimens to more accurately determine the distribution of this species in the country. However, there was a previous record of this species from Huanuco Department, in central Peru, south of the region of Iquitos (Eger, 2007). In Iquitos, most of the specimens were netted in urban areas. In a downtown building (Edificio EsSalud), the specimens were captured in a net placed in the 10th floor, where specimens ofMyotis albescensandP.macrotiswere also captured. Two other specimens were collected in the roof of a house where they were roosting with several specimens ofM. molossus. All other specimens were captured in a school, along withM.molossus,M.rufusandPhyllostomus hastatus. Only the specimens from Moena Ca?o were captured in a natural habitat, a secondary forest area, with elevated mist nets during the evening. At least 15 other species belonging to four families (Emballonuridae, Molossidae, Phyllostomidae, and Vespertilionidae) were also collected in this locality. Pregnant females were recorded on 24th November 2003, 24th March 2004, 3rd March 2005, and 5th July 2005, and a male with scrotal testicles was registered on 25th November 2003.

3 Discussion

The small mammals of the Amazon Basin of Peru have been the subject of numerous studies, but the attention has mainly focused on the southern and central parts of the country, particularly the Manu area (Terborgh et al, 1984; Janson & Emmons, 1990; Ascorra et al, 1991, 1996; Patterson et al, 1992, 1996, 1998, 2006; Pacheco et al, 1993, 1994; Pacheco & Vivar, 1996; Wilson & Sandoval, 1996; Zeballos-Patrón et al, 2001; Leite-Pitman et al, 2003; Bravo et al, 2008). Only a few studies have been conducted in the northeastern area (Sandborn, 1949; Thomas, 1924, 1927, 1928a, b; Ascorra et al, 1993), and specifically in Iquitos, including by members of our research group and colleagues (Davis & Dixon, 1976; Hice, 2003; Angulo & Díaz, 2004; Díaz & Willig, 2004; Hice et al, 2004; Willig et al, 2007). However, none of these investigations has included sampling in urban and suburban areas. As a consequence, my decision to include these areas in our surveys has resulted in the collection of several species recorded for the first time, as well as species newly added to the region and to the country.

Despite intensive sampling over several years, all of these new distributional records were obtained by capturing just a few specimens. Only single specimens were captured forA.caudifer,L. spurrelli,P.macrotis,E.delticus, andE.maurus. Two specimens ofV.spectrumand three ofC.planirostriswere obtained, and five specimens ofPeropteryxpallidopterawere captured from the roost at one locality. This reflects the low abundance of these species and indicates their rarity.Molossus coibensis, a widely distributed and very abundant species, was the only of the new species collected in this study that has been recorded by several specimens.LionycterisspurelliandPeropteryx pallidopterawere the only specimens collected in primary forest, a habitat where both species are frequently related (Handley, 1976; Lim et al, 2010). All other species were collected in somewhat modified environments, such as rural areas (Eumops delticus), suburban areas (Eumops maurus), secondary forestdeforested ecotones (Anoura caudifer), secondary forests (Molossus coibensis,Thyroptera lavaliandVampyrum spectrum), and urban areas (Peropteryx microtis,CynomopsplanirostrisandMolossus coibensis).

The presence ofT. lavaliin secondary forests was not known, and some authors (Reid et al, 2000; Solari et al, 2004) have indicated that “it seems to prefer primary forest near swamps”. In this study, the species was collected in a secondary forest patch surrounded by agricultural fields and flooded areas.A. caudiferandV. spectrumwere captured in secondary forests but these localities were surrounded by very large patches of wellpreserved forests. For example,V. spectrumwas captured in a locality close to the wildlife reserve of Allpahuayo Mishana. The presence of molossid bats in urban and suburban areas is well known; moreover, the presence of emballonurids in these environments is apparently more common than supposed. Several distributional range extensions and inclusions of new species in some countries were consequences of specimens collected in urban areas (Handley, 1976; Furlonger et al, 1987; Sodré & Uiedam, 2006; Dalponte & Aguiar, 2009; Mantilla-Meluk et al, 2009). It is possible that those specimens were attracted by roosting opportunities in buildings, or by the insects flying around the nearby street lamps (Dalponte & Aguiar, 2009).

It is well known that habitat modification for agricultural purposes (Aramburú, 1984; Hice, 2003; Willig et al, 2007) is one of the greatest threats to nature. This process has a negative effect on biodiversity, mainly because of the isolation imposed on environments and the resulting decrease in species richness and modification of population dynamics (Luque et al, 1994; Iida & Nakashizuka, 1995; Luque, 2000).

Habitat destruction, deforestation due to population pressure, the use of wood, and the exploitation of land for agricultural purposes were all observed during this study. In this context, it is necessary to state that bats are one of the groups of mammals most affected by habitat destruction and fragmentation (Cosson et al, 1999; Gorresen & Willig, 2004). The Iquitos region in particular, is a very distressed and fragmented area (Willig et al, 2007) and is included in the Peruvian Amazon forest, where approximately 0.4% (271,000 ha) is being converted to cropland or pasture each year (World Resources Institute, 1990).

Acknowledgements: My sincere gratitude to Victor Linares, Sixto Mananita, Harold Portocarrero, Cesar Ahuanari, Rubi Angulo, and to the students of the Universidad Nacional de San Marcos for their help with lab and fieldwork. Special gratitude goes to Rubén Barquez and William Lamar for their constant support, for help with the English corrections, and for his suggestion that improved this manuscript. Fieldwork was supported by the United States Public Health Service National Institute of Allergy and Infectious Diseases, USA (grants R01TW005860, D43TW007120, and K24AI068903). I especially thank Joseph Vinetz, the principal investigator on the grants that supported the fieldwork. I also thanks the Instituto Nacional de Recursos Naturales (INRENA) and the Ministerio de Agricultura of Peru for the permits to capture and collect specimens.

Alvarez Alonso J. 2002. Characteristic Avifauna of White-sand Forests in Northern Peruvian Amazonia[D]. M.Sc. Thesis, Louisiana State University and Agricultural and Mechanical College, Louisiana, USA, 96.

Angulo SR, Díaz MM. 2004. Nuevos registros deSphaeronycteris toxophyllumpara la cuenca Amazónica de Perú[J].Mastozool Neotrop, 11: 233-236.

Aramburú CE. 1984. Expansion of the Agrarian and Demographic Frontier in the Peruvian Selva[M]//Schmink M, Wood CH. Frontier Expansion in Amazonia. Gainesville: University of Florida Press, 153-179.

Ascorra CF, Wilson DE, Romo RM. 1991. Lista anotada de los quirópteros del Parque Nacional Manu, Perú. Publ. Mus Hist nat UNMSM(A)42:1-14.

Ascorra CF, Gorchov DL, Cornejo F. 1993. The bats from Jenaro Herrera, Loreto, Perú[J].Mammalia, 57: 533-552.

Ascorra CF, Solari S, Wilson DE. 1996. Diversidad y ecología de los quirópteros en Pakitza[M]// Wilson DE, Sandoval A. Manu, the Biodiversity of Southeastern Peru. Washington DC: Smithsonian Institution, 593-612.

Avila-Flores R, Fenton MB. 2005. Use of spatial features by foraging insectivorous bats in a large urban landscape[J].J Mamm, 86: 1193-1204.

Barquez RM, Mares AM, Braun JK. 1999. The Bats of Argentina: Special Editions [M]. Texas: Museum of Texas Tech University, 42: 1-275.

Bravo A, Harms KE, Stevens RD, Emmons LH. 2008. Collpas: Activity hotspots for frugivorous bats (Phyllostomidae) in the Peruvian Amazon[J].Biotropica, 40: 203-210.

Cosson J, Pons J, Masson D. 1999. Effect of forest fragmentation on frugivorous and nectarivorous bats in French Guiana[J].J Tropic Ecol, 15: 515-534.

Dalponte JC, Aguiar LMS. 2009. The first record ofDiclidurus ingensHernandez-Camacho, 1955 (Emballonuridae) in Central Brazil[J/OL].Biota Neotropical, 9(4): http://www.biotaneotropica. org.br/v9n4/en/abstract?short-communication+bn00409042009.

Davis WB, Dixon JR. 1976. Activity of bats in a small village clearing near Iquitos, Peru[J].J Mamm, 57: 747-749.

Díaz MM, Willig MR. 2004. Nuevos registros deGlironia venustayDidelphis albiventris(Didelphimorpia) para Perú[J].Mastozool Neotrop, 11: 185-192.

Díaz MM, Flores DA, Barquez RM. 1998. Instrucciones para la preparación y conservación de mamíferos. PIDBA (Programa de Investigaciones de Biodiversidad Argentina),Publicaciones Especiales, 1: 1-18.

Dolan PG. 1989. Systematics of Middle American mastiff bats of the genusMolossus: Special Publication[M]. Texas: The Museum, Texas Tech University, 29: 1-71.

Eger JL. 1977. Systematics of the genusEumops(Chiroptera: Molossidae) [J].Life Sci Contrib Royal Ontario Museum, 110: 1-69.

Eger JL. 2007. Family Molossidae[M]// Gardner AL. Mammals of South America. Volume 1. Marsupials, Xenarthrans, Shrews, and Bats. Chicago: The University of Chicago Press, 399-440.

Emmons LH. 1984. Geographic variation in densities of non-flying mammals in Amazonia[J].Biotropica, 16: 210-222.

Encarnación E. 1985. Introducción a la flora y vegetación de la Amazonía peruana: estado actual de los estudios, medio natural y ensayo de una clave de determinación de las formaciones vegetales en la llanura amazónica[J].Candollea, 40: 237-252.

Everette AL, O'Shea TJ, Ellison LE, Stone LA, McCance JL. 2001. Bats use of a high-plains urban wildlife refuge[J].Wildl Soci Bull, 29: 967-973.

Fenton M. 1997. Science and the conservation of bats[J].J Mamm, 78: 1-14.

Fleck DW, Voss RS, Simmons NB. 2002 Under differentiated taxa and sublexical categorization: An example from Matses classification of bats[J].J Ethnobiol, 22(1): 61-102.

Furlonger CL, Dewar HJ, Fenton MB. 1987. Habitat use by foraging insectivorous bats[J].Can J Zool, 65(2): 284-288.

Gentry AH. 1986. Endemism in Tropical Versus Temperate Plant Communities[M]//Soulé ME. Conservation Biology: the Science of Scarcity and Diversity. Sunderland, Massachusetts: Sinauer Associates, 153-181.

Gentry AH. 1988. Tree species richness of upper Amazonian forests[J].Proc Natl Acad Sci USA, 85: 156-159.

Goodwin GC, Greenhall AM. 1961. A review of the bats of Trinidad and Tobago: Descriptions, rabies infections, and ecology[J].Bull Am Mus Nat Hist, 122: 187-302.

Gorresen PM, Willig MR. 2004. Landscape responses of bats to habitat fragmentation in Atlantic Forest of Paraguay[J].J Mamm, 85: 688-697.

Griffiths TA, Gardner AL. 2007a. Subfamily Glossophaginae[M]// Gardner AL. Mammals of South America. Volume 1. Marsupials, Xenarthrans, Shrews, and Bats. Chicago: the University of Chicago Press, 224-244.

Griffiths TA, Gardner AL. 2007b. Subfamily Lonchophyllinae[M]// Gardner AL. Mammals of South America. Volume 1. Marsupials, Xenarthrans, Shrews, and Bats. Chicago: the University of Chicago Press, 244-255.

Handley CO. 1976. Mammals of the Smithsonian Venezuelan Project[J].Sci Bull Brigham Young Univ,Biol Ser, 20(5): 1-89.

Hice CL. 2003. The non-volant mammals on the Estación Biológica Allpahuayo assessment of the natural history and community ecology of a proposed reserve[D]. Ph.D. Thesis, Texas Tech University, Lubbock, 304.

Hice CL, Solari S. 2002. First record ofCentronycteris maximiliani(Fischer, 1829) from Peru and two additional records ofC.centralisThomas, 1912 from the southeastern part of the country[J].Acta Chiropterol, 4: 217-219.

Hice CL, Velazco PM, Willig MR. 2004. Bats of the Reserva Nacional Allapahuayo-Mishana, northeastern Peru, with notes on community structure[J].Acta Chiropterol, 6: 319-334.

Hood C, Gardner AL. 2007. Family Emballonuridae[M]//Gardner AL. Mammals of South America. Volume 1. Marsupials, Xenarthrans, Shrews, and Bats. Chicago: the University of Chicago Press, 188-207.

Iida S, Nakashizuka T. 1995. Forest fragmentation and its effect on species diversity in sub-urban coppice forests in Japan[J].For Ecol Manag, 73: 197-210.

Janson C, Emmons LH. 1990. Ecological structure of the non-flying mammal community at Cocha Cashu Biological Station, Manu National Park, Peru[M]//Gentry AH. Four Neotropical Rainorests. Yale: Yale University Press. 314-338.

Kalliola R, Flores Paitán S (eds.). 1998. Geoecología y Desarrollo amazónico; Estudio Integrado en la Zona de Iquitos, Perú[M]. Turku: Turun Yliopisto, 544.

Kalliola R, Puhakka M, Danjoy W (eds.). 1993. Amazonia Peruana Vegetación Húmeda Subtropical en el Lano Subandino: Proyecto Amazonia Universidad de Turku (PAUT) and Oficina Nacional de Evaluación de Recursos Naturales (ONERN)[M]. Finland: Jyv?skyl?, 265.

Klingbeil BT, Willig MR. 2009. Guild-specific responses of bats to landscape composition and configuration in fragmented Amazonian Rainforest[J].J Appl Ecol, 46: 203-213.

Koopman KF. 1993. Orden Chiroptera[M]// Wilson DE, Reeder DM. Mammals Species of the World: A Taxonomic and Geographic Reference. Washington: Smithsonian Institution Press, 134-232.

Lamar WW. 1997. Checklist and common names of the reptiles of the Peruvian lower Amazon[J].Herpet Nat Hist, 5(1): 73-76.

Leite Pitman R, Beck H, Velazco PM, Leite Pitman R, Pitman N, Alvarez P. 2003. Mamíferos terrestres y arbóreos de la selva baja de la Amazonía peruana: Entre los ríos Manu y Alto Purús[J].Centr Trop Conserv, 109-124.

Lim BK, Engstrom MD, Reid FA, Simmons NB, Voss RS, Fleck DW. 2010. A new species ofPeropteryx(Chiroptera: Emballonuridae) from western Amazonia with comments on phylogenetic relationships with the genus[J].Am Mus Novit, 3686: 1-20.

Luna L, Emmons L, Romo M, Cornejo Farfán A, Montambault JR. 2002. Mamíferos encontrados en el Santuario Nacional Pampas del Heath durante la expedición del RAP de 1996: Informes de las evaluaciones biológicas Pampas del Heath, Perú; Alto Madidi, Bolivia; y Pando, Bolivia[M]. Washington DC: Conservation International Bull Biol Assessment24, 66-70.

Luque S. 2000. Evaluating temporal changes using multispectral scanner and thematic mapper data on the landscape of a natural reserve: The New Jersey Pine Barrens, a case study[J].Int J Remot Sensing, 21: 2589-2611.

Luque S, Lathrop Jr. RG, Bognar JA. 1994. Temporal and spatial changes in the New Jersey Pine Barrens landscape[J].Landscape Ecol, 9: 287-300.

Mantilla-Meluk H, Baker RJ. 2006. Systematics of smallAnoura(Chiroptera: Phyllostomidae) from Colombia, with description of a new species[J].Occas Paper,Mus Texas Tech, 261: 1-18.

Mantilla-Meluk H, Jimenez-Ortega AM, Palacios L, Baker RJ. 2009. Unexpected finding ofDiclidurus ingens, Hernandez-Camacho, 1955 (Chiroptera, Emballonuridae), in the Colombian Biogeographic Chocó[J].Mastozool Neotrop, 16: 229-232.

Oprea M, Mendes P, Vieira TB, Ditchfield AD. 2009. Do wooded streets provide connectivity for bats in an urban landscape? [J].Biodiv Conserv, 18: 2361-2371.

Ortiz-S R. 1997. Iquitos region[M/OL]// Davis SD, Heywood VH, Herrera-MacBryde O, Villa-Lobos J, Hamilton A. Centres of Plant Diversity: A Guide and Strategy for Their Conservation. The Americas. Volume 3. Cambridge, Englan.: IUCN Publications Unit, http://botany.si.edu/projects/cpd/.

Pacheco V. 2002. Mamíferos del Perú[M]// Ceballos G, Simonetti JA. Diversidad y conservación de los mamíferos neotropicales CONABIO (Comisión Nacional para el Conocimiento y Uso de la Biodiversidad)-UNAM (Universidad Nacional Autónoma de México), México, D.F., 503-549.

Pacheco V, Solari S, Vivar E, Hocking P. 1994. La riqueza Biológica del Parque Nacional Yanachaga Chemillen[J].Magistri Doctoris, 7: 3-6.

Pacheco V, Patterson BD, Patton JL, Emmons LH, Solari S, Ascorra CF. 1993. List of mammals species known to occur in Manu Biosphere Reserve, Peru[J].Publicaciones del Museo de Historia Natural, Universidad Nacional Mayor de San Marcos,Serie A Zoología, 44: 1-12.

Pacheco V, Cadenillas R, Salas E, Tello C, Zeballos H. 2009. Diversidad y endemismo de los mamíferos del Perú[J].Rev Peru Biol, 16(1): 5-32.

Pacheco V, Vivar E. 1996. Annotated checklist of the non-flying mammals at Pakitza, Manu Reserve Zone, Manu National Park, Peru[M]//Wilson DE, Sandoval A. Manu, the Biodiversity of Southeastern Peru. Washington DC: Smithsonian Institution, 577-592.

Patterson BD, Stotz DF, Solari S. 2006. Mammals and birds of the Manu Biophere Reserve, Peru[J].Fieldiana: Zool, 110: 1-49.

Patterson BD, Patton JL, Emmons LH. 1992. Lista completa de especies de mamíferos que se habitan la Reserva de la Biosfera del Manu[M]// MacQuarrie K. Peru's Amazonian Eden: Manu National Park and Biosphere Reserve. Barcelona: Francis O. Patthey e hijos, 125-128.

Patterson BD, Pacheco V, Solari S. 1996. Distribution of bats along an elevational gradient in the Andes of south-eastern Peru[J].J Zool:London, 240: 637-68.

Patterson BD, Stotz DF, Solari S. Fitzpatrick JW, Pacheco V. 1998. Contrasting patterns of elevational zonation for birds and mammals in the Andes of southeastern Peru[J].J Biogeogr, 25: 593-607.

Pine RH. 1993. A new species ofThyropteraSpix (Mammalia: Chiroptera: Thyropteridae) from the Amazon Basin in northeastern Peru[J].Mammalia, 57: 213-215.

Reid FA, Engstrom MD, Lim, BK. 2000. Noteworthy records of bats from Ecuador[J].Acta Chiropterol, 2: 37-51.

Rodríguez LB, Duellman, WF. 1994. Guide to the Frogs of the Iquitos Region, Amazonian Peru[J].Univ Kansas Nat Hist Mus Publ, 22: 1-80.

Ruokolainen K, Tuomisto H. 1993. La vegetación de terrenos no inundables (tierra firme) en la selva baja de la Amazonia peruana[M]// Kalliola R, Puhakka M, Danjoy W. Amazonia peruana vegetación húmeda subtropical en el llano subandino Proyecto Amazonia Universidad de Turku (PAUT) and Oficina Nacional de Evaluación de Recursos Naturales (ONERN). Finland: Jyv?skyl?, 139-153.

Salo J, Kalliola R, Haekkinen I, Maekinen Y, Niemelae P, Puhakka M, Coley PD. 1986. River dynamics and the diversity of Amazon lowland forest[J].Nature, 322: 254-258.

Sanborn CC. 1937. American bats of the subfamily Emballonurinae[J].Field Mus Nat Hist,Zool Ser, 20: 321-354.

Sanborn CC. 1949. Mammals from the Rio Ucayali, Peru[J].J Mamm, 30: 277-288.

Simmons NB. 2005. Order Chiroptera[M]//Wilson DE, Reeder DM. Mammal Species of the World: A Taxonomic and Geographic Reference. 3rded. Baltimore: Johns Hopkins University Press, 312-529.

Sodré .M, Uieda W. 2006. First record of the ghost batDiclidurus scutatusPeters (Mammalia, Chiroptera, Emballonuridae) in S?o Paulo City, Brazil[J].Rev Bras Zool, 23(3): 897-898.

Solari S, Pacheco V, Vivar E. 1999. New geographic records of Peruvian bats.Rev Peru Biol, 6: 152-159.

Solari S, Van Den Bussche RA, Hoofer SR, Patterson BD. 2004. Geographic distribution, ecology, and phylogenetic affinities ofThyroptera lavaliPine 1993[J].Acta Chiropterol, 6: 293-302.

Tafur Rengifo L. 2001. Distrito Iquitos, Capital Iquitos [M]// Kanatari, Editorial CETA (Centro de Estudios Teológicos de la Amazonía), Iquitos,. 131-152.

Terborgh J, Fitzpatrick JW, Emmons LH. 1984. Annotated checklist of bird and mammal species of Cocha Cashu Biological Station, Manu National Park, Peru[J].Fieldiana Zool,New Series, 21: 1-29.

Thomas O. 1924. On a collection of mammals made by Mr. Latham Rutter in the Peruvian Amazons[J].Ann Mag Nat Hist, 9: 530-538.

Thomas O. 1927. On mammals collected by Mr. R. W. Hendee in the Province of San Martin, N. Peru, mostly at Yurac Yacu[J].Ann Mag Nat Hist, 9(19): 361-375.

Thomas O. 1928a. The mammals of the Rio Ucayali[J].Ann Mag Nat Hist, 10(2): 249-265.

Thomas O. 1928b. On mammals obtained by Mr. Hendee at Pebas and Iquitos[J].Ann Mag Nat Hist, 10(2): 286-294.

Tirira, D. 2006. Mamíferos del Ecuador, Diversidad:Eumops maurus(Thomas, 1901) [DB/OL]. Website page (January 2006). Versión 1.1. Ediciones Murciélago Blanco. Quito. ＜http://www.terraecuador. net/mamiferosdelecuador/diversidad.htm＞ [Asssesed at 2008-07-10]

Tuomisto H, Roukolainen K, Kalliola R, Linna A, Danjoy W, Rodríguez Z. 1995. Dissection Amazonian Biodiversity[J].Science, 269: 63-66.

Voss RS, Emmons LH. 1996. Mammalian diversity in Neotropical lowland rainforest: A preliminary assessment[J].Bull Am Mus Nat Hist, 210: 1-113.

Williams SL, Genoways HH. 2007. Subfamily Phyllostominae[M]// Gardner AL. Mammals of South America. Volume 1. Marsupials, Xenarthrans, Shrews, and Bats. Chicago: the University of Chicago Press, 255-300.

Willig MR. 1983. Composition, microgeographic variation, and sexual dimorphism in Caatingas and Cerrado bat communities from northeastern Brazil[J].Bull Carnegie Mus Nat Hist, 23: 1-131.

Willig MR, Presley SJ, Bloch CP, Hice CL, Yanoviak SP, Díaz MM, Arias Chauca L, Pacheco V, Weaver SC. 2007. Phyllostomid bats of lowland Amazonia: Effects of habitat alteration on abundance[J].Biotropica, 39: 737-746.

Wilson DE. 2007. Family Thyropteridae[M]// Gardner AL. Mammals of South America. Volume 1. Marsupials, Xenarthrans, Shrews, and Bats. Chicago: the University of Chicago Press, 392-396.

Wilson DE, Sandoval A (eds.) 1996. Manu: The Biodiversity of Southeastern Peru[M].Lima, Peru: Smithsonian Institution Press. Woodman N, Timm RM. 2006. Characters and phylogenetic relationships of nectar-feeding bats, with descriptions of the newLonchophyllafrom western South America (Mammalia: Chiroptera: Phyllostomidae: Lonchophyllini) [J].Proc Biol Soc Washington, 119(4): 437-476.

World Resources Institute. 1990. World Resources 1990 - 1991:. World Resources Institute, Washington, DC, in collaboration with the United Nations Environment Program and the United Nations Development Program[M] Cambridge, UK: Oxford University Press.

Yee DA. 2000. Peropteryx macrotis[J].Mamm Species, 643: 1-4.

Zeballos-Patrón H, Pacheco V, Baraybar L. 2001. Diversidad y conservación de los mamíferos de Arequipa, Perú[J].Rev Peru Biol8(2): 94-104.

Appendix I

List of localities, district and province in brackets, geographic coordinates, and type of habitat.

1. 1 km E km 25.3 de la carretera Iquitos-Nauta (Fundo San Martín) (San Juan) 3° 57.954' S 73° 24.259' W—Tropical humid forest.

2. app. 500 m E km 28.8 de la carretera Iquitos-Nauta (San Juan) 3° 59.227' S 73° 24.920' W—Tropical humid forest.

3. Asociación de Viviendas 15 de Mayo (E Av. Qui?ones) (San Juan) 3° 45.903' S 73° 17.725' W—Suburban area.

4. Camino a El Paujil, 1,8 km al W del km 35 de la carretera Iquitos-Nauta (San Juan) 4° 01.217' S 73° 26.787' W—Tropical humid forest.

5. Colegio Primario Secundario “RADM” (Rosa Agustina Donayre de Morey), calle Putumayo (Iquitos) 3° 44.997' S 73° 15.137' W—Urban area.

6. El Dorado, km 25 de la carretera Iquitos-Nauta, app. 1.5 km al E (San Juan) 3° 58.010' S 73° 23.620' W—Ecotone deforested area and secondary forest.

7. Iquitos, Edificio EsSalud (calles Raymondi-Napo) (Iquitos) 3° 44.942' S 73° 14.613' W—Urban area.

8. km 25 de la carretera Iquitos-Nauta (Fundo San Martín) (San Juan) 3° 57.954' S 73° 24.259' W—Secondary forest.

9. Moena Ca?o (Belén) 3° 46.728' S 73° 13.495' W—Secondary forest.

10. Piscina Olímpica del Instituto Peruano de Deportes, km 1.5 al W de la carretera Iquitos-Nauta (San Juan) 3° 47.696' S 73° 18.231' W—Rural area.

11. Puerto Indiana, Amazon River (Indiana) 03° 43.05' S 73° 04.32' W.

12. Punchana, Calle Amazonas 1086 (casa de Dr. Gendrau) (Punchana) 3° 43.506' S 73° 15.113' W—Urban area.

13. Villa del Ejército (entre Av. 28 de Julio-Freyre y calle Piura) (Punchana) 3° 43.658' S 73° 14.608' W—Urban area.

14. Zungarococha, 5.4 km al W del km 6 de la carretera Iquitos-Nauta (San Juan) 3° 49.825' S 73° 22.288' W—Secondary forest.

秘魯亞馬孫北部地區(qū)蝙蝠新記錄

M Mónica Díaz*

[PIDBA (Program of Argentine Biodiversity Research), Faculty of Natural Science and Institute Miguel Lillo, National University of Tucuman-PCMA (Program of Argentine Bat Conservation);CONICET (National Council of Scientific and Technical Research), Miguel Lillo 205, CP. 4000, Tucumán, Argentina]

位于秘魯?shù)膩嗰R孫盆地北部是世界小型哺乳動(dòng)物多樣性最高的地區(qū)之一。該文報(bào)道了亞馬孫流域在秘魯伊基托斯的蝙蝠物種多樣性：這里的蝙蝠物種數(shù)約占秘魯已知152個(gè)蝙蝠物種的60%。與在該地區(qū)之前開(kāi)展的研究不同, 本次調(diào)查范圍為城市和農(nóng)村地區(qū)。結(jié)果發(fā)現(xiàn) 1個(gè)秘魯新記錄(Eumops delticus)、8個(gè)伊基托斯新記錄(Peropteryx macrotis、Peropteryx pallidoptera、Anoura caudifer、Lionycteris spurrelli、Vampyrum spectrum、Thyroptera lavali、Cynomops planirostris和Molossus coibensis)和1個(gè)秘魯東北部新記錄(Eumops maurus)。

翼手目; 伊基托斯; 亞馬孫; 記錄

Q959.833； Q959.833.09

A

0254-5853-(2011)02-0168-11

2010-08-12；接受日期：2011-02-28

10.3724/SP.J.1141.2011.02168

date: 2010-08-12; Accepted date: 2011-02-28

*Corresponding author (通信作者), Email: mmonicadiaz@arnet.com.ar