Mammalian diversity in the Savanna from Peru, with three new addictions from country

  • Cesar Edgardo Medina Museo de Historia Natural de la Universidad Nacional de San Agustín de Arequipa (MUSA)
  • Kateryn Pino Museo de Historia Natural de la Universidad Nacional de San Agustín de Arequipa (MUSA)
  • Alexander Pari Museo de Historia Natural de la Universidad Nacional de San Agustín de Arequipa (MUSA)
  • Gabriel Llerena Museo de Historia Natural de la Universidad Nacional de San Agustín de Arequipa (MUSA)
  • Horacio Zeballos Pontificia Universidad Católica del Peru Instituto de Ciencias de la Naturaleza, Territorio y Energías Renovables
  • Evaristo López Museo de Historia Natural de la Universidad Nacional de San Agustín de Arequipa (MUSA) Facultad de Ciencias Biológicas y Agropecuarias de la Universidad Nacional de San Agustín de Arequipa

Abstract

Bahuaja Sonene National Park protects the unique sample of subtropical humid savannas in Peru, which are known as “Pampas del Heath” with 6,136 hectares of area. Many endangered species and/or endemic from savannas occur there, however studies about the diversity of mammals in Pampas del Heath are limited and only three assessments there have been carried out since mid‑1970s. Therefore we surveyed mammals in three habitat types of the Pampas del Heath (savanna, ecotonal area and forest) during late 2011. We used several methods of record for the different mammal groups including 1) capture techniques with mist nets, snap traps, Sherman traps, Tomahawk traps and pitfall traps, 2) and detection techniques direct by means of camera traps, visualization of mammals during long walk, observation of tracks and interviews to local people. Total capture efforts totalized 6,033 trap/nights, 136 mist-net/nights and 108 cameras/nights. Sixty-nine species of mammals were recorded: 33 in savanna, 33 in ecotonal area and 38 in forest. Sixteen species are new records for the Pampas del Heath and three are new records from Peru (Cryptonanus unduaviensis, Rhogeessa hussoni and Rhogeessa io). Analyses on the sampling effort, relative density, diversity and community structure of small mammals were made for the three habitats types. Moreover eight species are Threatened and 24 are listed in CITES. The new records here presented elevated the previous known mammal species richness in Peru from 538 to 541, and show the importance to conduct inventories to describe the biodiversity in remote areas, like the Pampas del Heath.

Downloads

Download data is not yet available.
Published
2016-09-28
How to Cite
Medina, C., Pino, K., Pari, A., Llerena, G., Zeballos, H., & López, E. (2016). Mammalian diversity in the Savanna from Peru, with three new addictions from country. Papéis Avulsos De Zoologia, 56(2), 9-26. https://doi.org/10.1590/0031-1049.2016.56.02
Section
Original Article

INTRODUCTION

The Cerrado Biome includes an array of forests and savannas that border the southern edge of the Amazon rain forest, located mainly in central Brazil, eastern Bolivia and some parts of Paraguay. These habitats have tropical climates with strong temperature, rainfall seasonality, nutrient-poor, poorly drained areas subject to annual flooding and desiccation support edaphic, fire- and flood-maintained grasslands, and savanna woodlands (Gottsberger & Silberbauer-Gottsberger, 2006).

The Bahuaja Sonene National Park (PNBS) protect the Pampas del Heath since 1996. These are the unique sample of savanna within Peruvian territorial limits, and home to many species known nowhere else in the country, such as the Maned Wolf Chrysocyon brachyurus and the Marsh Deer Blastocerus dichotomus (Hofmann et al., 1976; Luna et al., 2002). Studies about the diversity of mammals in Pampas del Heath are sparse and only three assessments there are since the mid-1970s to nowadays (Hofmann et al., 1976; Emmons et al., 1994; Luna et al., 2002), which reduced the successful management of this protected area.

Under this premise the “Asociación para la Investigación y el Desarrollo Integral” (AIDER), the “Museo de Historia Natural de la Universidad Nacional San Agustín de Arequipa” (MUSA) and “Servicio Nacional de Áreas Naturales Protegidas por el Estado” (SERNANP) together made possible carry out an important expedition to the Pampas del Heath in 2011 in order to fill this information gaps. This paper documented the diversity of mammals of three localities placed in Pampas del Heath, according to three habitats types (savanna, ecotonal area and forest).

MATERIALS AND METHODS

Study area

The Pampas del Heath is located in the Madre de Dios Department, southeastern Peru, near border between Peru and Bolivia (Figure 1). It has an area of 6,136 hectares (MINAM, 2012), and it is an extension of Cerrado Paceño (Ibisch et al., 2003) with a warm, humid and tropical climate (Hanagarth & Beck, 1996). Precipitation annual is approximately 2,000 mm and average temperature is between 24 and 26°C (Luna et al., 2002).

Location of Pampas del Heath from Peru: (1) Aguas Claras Camp; (2) Cocha Paujil; and (3) Refugio Juliaca. The gray area represents the Savanna (from Josse et al., 2007).

FIGURE 1:: Location of Pampas del Heath from Peru: (1) Aguas Claras Camp; (2) Cocha Paujil; and (3) Refugio Juliaca. The gray area represents the Savanna (from Josse et al., 2007).

The savanna in this region is characterized by herbaceous vegetation composed mainly of Poaceae and Ciperaceae, occurring together with termite mounds surrounded by clayey poorly drained soils. Palms (Mauritia flexuosa) may also occur in the area either dispersed or concentrated along of marshes and forming Gallery forests (Figure 2). There are also patch forests like small islands of 100 m2 composed by shrubs such plant of the family Melastomataceae (Macairea thyrsiflora, Graffenrieda limbata, between others) and small tree (Matayba guianensis, Virola sebifera, between others) (MINAM, 2012).

Panoramic views of the Pampas del Heath from Peru (top) with patches of forests (middle) and palms (bottom).

FIGURE 2:: Panoramic views of the Pampas del Heath from Peru (top) with patches of forests (middle) and palms (bottom).

This mosaic of savannas is surrounded by seasonal evergreen Amazonian forests, with a canopy that reaches 30-35 m and emergent of up to 40 m, and the frequent presence of Bertholletia excelsa. The forest develops on well-drained soils of the lateritic rolling pen plain of the southwestern Amazon, where it represents the extensive matrix of vegetation cover in areas with humid pluviseasonal bioclimate of southern Peru, northern Bolivia and western Brazil (Josse et al., 2007).

The ecotonal area between the savanna and forest has a variable size that could be of a few meters in burned areas, until 80 m in unburned area.

We surveyed mammals in three localities of the Pampas del Heath at the beginning of wet season, since 30 November to 14 December 2011, which are following:

  1. Aguas Claras Camp (-12°57’20”S, -68°54’46”W, 216 m), located in a patch of forest inserted in the savanna (Figure 1). The surveys were carried out during 14 continuous days installing traps in two habitats (savanna and ecotonal area).

  2. Cocha Paujil (-12°53’33”S, -68°53’12”W, 218 m), located to approximately 7 km northeast Aguas Claras Camp. The surveys were carried out the last four days of the expedition installing traps in the ecotonal area habitat.

  3. Refugio Juliaca (-12°57’19”S, -68°53’08”W, 211 m), located next to Heath River. The surveys were carried out during 10 continuous days installing traps in the forest habitats.

Field methods

Marsupials and rodents were caught in Pitfall traps, Victor traps, Sherman traps and Tomahawk traps (Aplin et al., 2003). Pitfall traps were installed in two transects of 60 m with 10 buckets of five gallons each one and with drift fences (Voss & Emmons, 1996; Patton et al., 2000) which were checked every 12 hours. Other traps were placed in two transects of one km in length each one and that were used a bait composed of oat, vanilla and canned fish. In the forest, Victor traps were installed both on ground as to 1.5 m of height, meanwhile Tomahawk traps were installed at different heights (cero, two, eight and 15 m) following to Graipel (2001) but with some modifications, and these used as bait banana essence.

Bats were registered with mist nets standard, 12 m long by 2.5 m high, which were installed in different places of frequent passage by bats and to different heights, from level ground to 30 m, between palms. The mist nets were open from 18:00 until 6:00 hours and were checked regularly during the night. Additionally, we searched for bats in their shelters, such as hollow trees, under leaves, among others (Jones et al., 1996).

Cuddeback camera traps with motion detection sensors were used in savanna following a trapping opportunistic methodology regarding the location and number of cameras. Cameras were separated by one to three km from each other, arranged on possible paths of the animals and programmed to take all day with a minimum interval of one minute between photos. Walks were made for observation and traces search of large mammals (feces, burrows, tracks, bones, etc.) which were performed at a speed of about one km/hour. Moreover interviews were conducted at park rangers following to Dietrich (1995) and with the support of color plates of species potentially present in the study area (Emmons & Feer, 1999; Eisenberg & Redford, 1999; Leite et al., 2009).

Specimens were collected as material reference being preserved as skins or fluid following to López et al. (1998) and these were deposited in the Scientific Collection of Museo de Historia Natural de la Universidad Nacional de San Agustin (MUSA).

Data analyses

Captured or photographed specimens and different tracks founded in field were identified with taxonomic keys (Anderson, 1997; Emmons & Feer, 1999; Gardner, 2007a; Voss & Jansa, 2009; Weksler & Percequillo, 2011), specialized literature (Patton et al., 2000; Rossi, 2005; Percequillo et al., 2008; Leite, 2009) and by comparison with housed specimen in MUSA. Taxonomy follows Pacheco et al. (2009).

Specimens representing new records for Peru were analyzed and compared with diagnostic characters and measurements available in the literature (Goodwin, 1958; LaVal, 1973; Ruedas & Bickham, 1992; Voss et al., 2005; Bickman & Ruedas, 2007; Gardner, 2007b; Aires et al., 2011; Baird et al., 2012). Measurements obtained for each specimen include external measurements from tags or field notes: total length (TL), length of tail (LT), length of hind foot (HF), length of ear (Ear), length forearm only for bats (FA) and weight (W); head-and-body length was computed (HBL) by subtracting LT from TL. All measurements are in millimeter (mm) and weights are in gram (g). Cranial and mandibular measures were taken with help of a digital caliper to the nearest 0.01 mm. Marsupials were measured following definitions and illustrations of Voss et al. (2001, 2005). Vespertilionidae family bats were measured following LaVal (1973), and Ruedas & Bickham (1992) with some modifications by Baird et al. (2012).

Species accumulation curves for small mammals based on Clench model were calculated to determine if the sampling effort was adequate (Soberón & Llorente, 1993; Moreno, 2001). The randomization of the data was performed with Primer v.6 program (Clarke & Gorley, 2006), while the curves were drawn in Statistica v.7 program (StatSoft, 1998) with the adjustment method Simplex & Quasi-Newton (Jiménez-Valverde & Hortal, 2005).

Relative density of small mammals was estimated by Trap-Day Index which relates the number of individuals caught with the capture effort employed (Calhoum & Casby, 1958). For bats, the Index expresses the number of individuals captured (including those released) per 10 mist-net/nights, while for marsupials and rodents the number of individuals caught per 100 trap/nights.

The diversity of small mammals was analyzed with the Margalef (DMg) and the Menhinick (DMn) index based on data submitted previously to rarefaction (Magurran, 1988) while the community structure based on range-abundance curves (Feinsinger, 2001; Moreno, 2001). Trophic groups were assigned following Emmons & Feer (1999), Hice et al. (2004), do Nascimento (2007), Percequillo et al. (2008) and Guichón & Cassini (2009).

The conservation status of each species recorded was evaluated according to the criteria adopted by national and international institutions (MINAGRI, 2014; IUCN, 2012; CITES, 2013). Endemic species were assigned following Pacheco et al. (2009).

RESULTS AND DISCUSSION

During 15 days of survey, we used 136 mist-nets (59 in savanna, 47 in ecotonal area and 30 in Forest), 6,033 traps-nights (2,925 in savanna, 2,287 in ecotonal area and 1,599 in forest) and 108 camera-nights (all in savanna) in sampling for a total of 331 small mammals caught and two large mammals photographed. The capture effort was larger than previous assessments in the Pampas del Heath (Emmons et al., 1994; Luna et al., 2002).

Richness

We reported 69 species of mammals, which belong to nine orders, 24 families and 55 genera (Table 1). The families Phyllostomidae (15 species) and Cricetidae (10 species) were the best represented following of Didelphidae (nine species), Molossidae (six species) and Vespertilionidae (six species).

TABLE 1::
Mammals registered in Pampas del Heath (Bahuaja Sonene National Park). New records from the Area is denoted with triangles, meanwhile new records from Peru is with squares. Numbers in brackets include the relative densities of small mammal species. Previous records: α, Emmons et al. (1996); and β, Luna et al. (2002). Trophic Group: Fu, Fungivorous; In, Insectivorous; Fr, Frugivorous; Gr, Granivorous; He, Herbivorous; Cr, Carnivorous; Om, Omnivorous; Ne, Nectarivorous.
Code Species Accounts Common names   Vegetation forms   Previous records Trophic Group
      Savanna Ecotone Forest    
  DIDELPHIMORPHIA            
  Didelphidae            
  Caluromys lanatus Brown-eared Woolly Opossum       α, β Fr, In
A Cryptonanus unduaviensis ▲■ Unduave Mouse Opossum   X (0.04)     In, Fr
  Didelphis marsupialis Common Opossum     X α, β Om
B Lutreolina crassicaudata Lutrine Opossum X (0.03)     β Cr
C Marmosa lepida Rufous Mouse Opossum   X (0.04)     In, Fr
  Marmosa murina Murine Opossum       β In, Fr
D Marmosa (Micoureus) regina Bare-tailed Woolly Mouse Opossum   X (0.04)   α, β Om
E Monodelphis peruviana Peruvian Short-tailed Opossum   X (0.17) X (0.19) β In
F Marmosops bishopi Bishop’s Slender Opossum   X (0.09) X (0.31)   In, Fr
G Marmosopssp. ▲ Slender Opossum X (0.03) X (0.13) X (0.13)   In, Fr
  Marmosops impavidus Tschudi’s Slender Opossum       β In, Fr
H Marmosops noctivagus White-bellied Slender Opossum     X (0.06) α In, Fr
  Philander opossum Gray Four-eyed Opossum       α, β In, Cr
  CINGULATA            
  Dasypodidae            
  Dasypus novemcinctus Nine-banded Armadillo X     β In, Cr
  Dasypus cf. septemcinctus Brazilian Lesser Long-nosed Armadillo       α In
  Priodontes maximus Giant Armadillo     X α In
  PILOSA            
  Myrmecophagidae            
  Myrmecophaga tridactyla Giant Anteater       α In
  Tamandua tetradactyla Southern Tamandua       β In
  PRIMATES            
  Cevidae            
  Cebus albifrons White-fronted Capuchin   X   β Fr, In
  Saguinus fuscicollis Brown-mantled Tamarin       α, β Fr, Ne, In
  Saguinus imperator Emperor Tamarin       β Fr, Ne, In
  Aotus azarae Azara’s Night Monkey     X α, β Fr, In, Ne
  Saimiri sciureus Tufted Capuchin       α, β In, Fr, Ne
  Sapajus apella Guianan/margarita Island Brown Capuchin       α, β Om
  Pitheciidae            
  Callicebussp. Titi   X   α, β He, Fr
  Atelidae            
  Alouatta sara Bolivian Red Howler     X α, β Fr, He
  Ateles chamek Peruvian Spider Monkey       α Fr, He
  RODENTIA            
  Sciuridae            
  Sciurus ignitus Bolivian Squirrel       α Gr, Fr, Fu
  Sciurus sanborni Sanborn’s Squirrel       α Gr
  Sciurus spadiceus Southern Amazon Red Squirrel   X   α, β Gr, Fr
  Cricetidae            
I Cerradomys maracajuensis Maracaju’s Rice rat X (0.21) X (0.26)   α, β He, In
J Euryoryzomys nitidus Elegant Oryzomys X (0.03) X (0.31) X (0.50)   Fr, In, Gr
K Hylaeamys perenensis Western Amazonian’s Rice Rat X (0.07) X (0.39) X (0.50) α, β Fr, In, Gr
L Pseudoryzomys simplex Brazilian False Rice Rat X (0.79) X (0.04)   β ¿?
M Neacomys minutus Tiny Bristly Mouse   X (0.04) X (0.06)   In, Fr
N Neacomys spinosus Bristly Mouse   X (0.04) X (0.13)   In, Fr
O Necromys lenguarum Bolo Mouse X (2.70) X (0.22)   α, β In, Om
P Oecomys bicolor White-bellied Oecomys   X (0.13) X (0.19) α, β Fr, Gr
Q Oligoryzomys microtis Small-eared Pygmy Rice Rat   X (0.04)   β Gr, In
R Oligoryzomyssp. ▲ Pygmy Rice Rat X (0.03)       Gr, In
  Dinomyidae            
  Dinomys branickii Pacarana       α He
  Caviidae            
S Cavia aperea Brazilian Guinea Pig X (0.21)     α, β He
  Hydrochoerus hydrochaeris Capybara     X α, β He
  Dasyproctidae            
  Dasyprocta variegata Brown Agouti       α Fr, In
  Echimyidae            
  Mesomys hispidus Ferreira’s Spiny Tree Rat       α Fr, In
T Proechimys simonsi Simons’ Spiny-Rat   X (0.31) X (0.25) α, β Gr, Fr, Fu
  CHIRÓPTERA            
  Emballonuridae            
  Rhynchonycteris naso Proboscis Bat     X α, β In
  Saccopteryx bilineata Greater Sac-winged Bat       β In
  Peropteryx macrotis Lesser Dog-like Bat       β In
  Phyllostomidae            
U Glossophaga soricina Pallas’s Long-tongued Bat X (0.17) X (1.06) X (0.33) α Ne, In, Fr
  Lonchophylla thomasi Thomas’s Nectar Bat       α Ne, In
  Lophostoma silvicolum White-throated Round-eared Bat       α, β In, Fr
  Chrotopterus auritus Woolly False Vampire Bat       α Cr, In
  Micronycteris megalotis Little Big-eared Bat       α In, Fr
V Micronycteris minuta Tiny Big-eared Bat     X (0.33)   In, Fr
  Phyllostomus elongatus Lesser Spear-nosed Bat       α, β Fr, In, Ne
  Phyllostomus hastatus Greater Spear-nosed Bat       α, β Fr, In, Ne
  Tonatia saurophila Stripe-headed Round-eared Bat       β In, Fr
W Trachops cirrhosus Fringe-lipped Bat   X (0.21)   α Cr, In
  Carollia benkeithi Southern Chesnut Short-tailed Bat       α, β Fr, In, Ne
X Carollia brevicauda Silky Short-tailed Bat   X (0.21) X (0.67) α, β Fr, In, Ne
Y Carollia perspicillata Seba’s Short-tailed Bat X (0.34) X (0.85) X (0.33) α, β Fr, In, Ne
Z Rhinophylla pumilio Dwarf Little Fruit Bat     X (0.33) α, β Fr, In, Ne
AA Artibeus gnomus Dwarf Fruit-eating Bat X (0.17) X (0.21) X (1.33) α, β Fr
AB Artibeus lituratus Great Fruit-eating Bat X (2.20) X (0.64) X (1.33) α Fr, In, Ne
AC Artibeus obscurus Dark Fruit-eating Bat   X (0.21) X (1.33) α, β Fr, In, Ne
AD Artibeus planirostris Flat-faced Fruit-eating Bat X (0.34) X (0.21) X (1.33) α Fr, In, Ne
  Chiroderma trinitatum Little Big-eyed Bat       β Fr, In, Ne
  Chiroderma villosum Hairy Big-eyed Bat       α Fr, In, Ne
  Mesophylla macconnelli MacConnell’s Bat       α Fr, In, Ne
AE Platyrrhinus incarum Inca Broad-nosed Bat X (0.17)       Fr, In, Ne
  Sturnira lilium Little Yellow-shouldered Bat       α, β Fr, In, Ne
  Sturnira magna Greater Yellow-shouldered Bat       α Fr, In, Ne
AF Sturnira tildae Tilda’s Yellow-shouldered Bat     X (0.33) α, β Fr, In, Ne
AG Uroderma bilobatum Common Tent-making Bat X (0.85) X (0.21) X (0.33) α, β Fr, In, Ne
AH Uroderma magnirostrum Brown Tent-making Bat X (0.34) X (0.64)   α Fr, In, Ne
AI Vampyriscus bidens Bidentate Yellow-eared Bat   X (0.21) X (0.67) α Fr, In, Ne
  Vampyrodes caraccioli Great Stripe-faced Bat       α Fr, In, Ne
  Noctilionidae            
AJ Noctilio albiventris Lesser Bulldog Bat X (0.34)     α, β In
  Molossidae            
AK Cynomops abrasus Cinnamon Dog-faced Bat X (0.34)       In
AL Eumops maurus Guianan Bonneted Bat X (0.51)     β In
AM Eumops patagonicus Patagonian Bonneted Bat X (1.02)       In
AN Molossus coibensis Coiban Mastiff Bat X (0.51)       In
AO Molossus molossus Pallas’s Mastiff Bat X (0.17)   X (1.33) α, β In
AP Promops centralis Crested Mastiff Bat X (0.51)     β In
  Vespertilionidae            
  Eptesicus brasiliensis Brazilian Brown Bat       α, β  
AQ Eptesicus furinalis Argentinian Brown Bat X (0.51)     β In
AR Myotis albescens Silver-tipped Myotis     X (0.33) β In
AS Myotis nigricans Black Myotis X (1.86)     α In
AT Myotis riparius Riparian Myotis X (0.17)     α, β In
  Lasiurus cinereus Hoary Bat       β  
AU Rhogeessa hussoni ▲■ Eastern Little Yellow Bat X (0.17)       In
AV Rhogeessa io ▲■ Southern Little Yellow Bat   X (0.21)     In
  CARNIVORA            
  Felidae            
  Leopardus pardalis Ocelot       β Cr
  Leopardus wiedii Margay       α Cr, In
  Panthera onca Jaguar     X α, β Cr
  Puma concolor Cougar       β Cr
  Canidae            
  Atelocynus microtis Short-eared Dog     X α, β Cr
  Chrysocyon brachyurus Maned Wolf X     α, β Cr, Fr
  Mustelidae            
  Eira barbara Tayra       α, β Cr, In, Fr
  Lontra longicaudis Neotropical Otter     X β Cr, In
  Pteronura brasiliensis Giant Otter     X α, β Cr
  Procyonidae            
  Bassaricyon alleni Allen’s Olingo     X   Fr, In
  Nasua nasua South American Coati       α, β Om
  Potos flavus Kinkajou     X α, β Fr, In
  PERISSODACTYLA            
  Tapiridae            
  Tapirus terrestres South American Tapir X X X α, β He, Fr
  ARTIODACTYLA            
  Tayassuidae            
  Pecari tajacu Collared Peccary X X   α, β Fr, In, Cr
  Tayassu pecari White-lipped Peccary       α, β Fr, In
  Cervidae            
  Blastocerus dichotomus Marsh Deer X     α, β He
  Mazama americana South American Red Brocket     X α, β Fr, Fu
  Mazama nemorivaga South American Brown Brocket       α, β Fr
  Total orders   7 6 8    
  Total families   12 10 17    
  Total genera   27 25 32    
  Total species   33 33 38    

The forest had the highest raw species richness, followed by ecotonal area and savanna (38, 33 and 33 species, respectively). Likewise, 18 species were recorded only in the savanna while nine were in the ecotonal area and 20 in the forest. In contrast, ten species were common in all three vegetation forms (Table 1).

Sixteen species represented new records for the Pampas del Heath (Cryptonanus unduaviensis, Marmosa lepida, Marmosops bishopi, Marmosops sp., Euryoryzomys nitidus, Neacomys minutus, Neacomys spinosus, Oligoryzomys sp., Micronycteris minuta, Platyrrhinus incarum, Cynomops abrasus, Eumops patagonicus, Molossus coibensis, Rhogeessa hussoni, Rhogeessa io, and Bassaricyon alleni) (Figure 3).

Some species registered in Pampas del Heath from Peru: (A) Lutreolina crassicaudata˅; (B) Cryptonanus unduaviensis*; (C) Rhogeessa hussoni*; (D) Eumops patagonicus*; (E) Cavia aperea*; and (F) Chrysocyon brachyurus* (Photos by K. Pino˅ and A. Pari*).

FIGURE 3:: Some species registered in Pampas del Heath from Peru: (A) Lutreolina crassicaudata˅; (B) Cryptonanus unduaviensis*; (C) Rhogeessa hussoni*; (D) Eumops patagonicus*; (E) Cavia aperea*; and (F) Chrysocyon brachyurus* (Photos by K. Pino˅ and A. Pari*).

The outstanding records were three species unknown to the list of mammals from Peru, which are:

ORDER DIDELPHIMORPHIA Gill 1872

Family Didelphidae Gray 1821

Cryptonanus unduaviensis (Tate 1931)

Unduave Mouse Opossum

Specimen examined: adult female (MUSA 12695), collected at Aguas Claras Camp, Pampas del Heath, Madre de Dios (12°57’20”S, 68°54’46”W, 216 m). Measures see Table 2.

TABLE 2::
Measurements (mm) and weights (g) of the specimen of Cryptonanus unduaviensis from Peru and referred material to C. unduaviensis (data from Voss et al. 2005).
        Bolivia         Peru
  Santa Cruz   La Paz   Beni     Pando Madre de Dios
  IGP 157 MSB 58508 AMNH 72563 1 AMNH 209156 MSB 70752 AMNH 209154 FMNH 114658 MSB 57000 MUSA 12695
Sex m m m f f m m m f
Head-body length 1212 86 102 97 111 106 110 105 96
Total length 135 120 120 112 112 132 115 133 119
Length of hind foot 18 17 17 17 16 17 15 19 17.2
Length of ear 18 14 -   14 16 17 17 17
Condylobasal length 30 25.9 - 25.6 26.9 28.2 - 28.3 26.3
Nasal breadth 4.4 3.3 3.3 3.5 3.7 4.2 3.5 4.2 3.7
Least interorbital breadth 5.3 4.8 - 4.7 4.6 5.2 4.9 5 4.8
Zygomatic breadth 17.6 14.7 - 14.2 15.3 15 - 16.3 14.8
Palatal length 16.2 14.2 - 14.1 14.6 15.7 14.8 15.5 14.5
Palatal breadth 9.6 8.4 - 8.2 8.3 8.1 8.6 8.3 8.6
Maxillary toothrow length 11 10.5 10.9 10.3 10.5 10.9 10.7 10.7 10.5
Length of molars 5.7 5.7 5.7 5.6 5.6 5.7 5.8 5.6 5.7
Length of M1-M3 4.9 4.9 4.9 4.8 4.8 5 5.1 4.8 4.9
Weight 40 15 - 18 21 24 28 26 22

1 holotype; 2 atipical measure.

Remarks: The genus Cryptonanus contains five species distributed in Bolivia, Brazil, Paraguay, Argentina and Uruguay (Tate, 1931; Voss et al., 2005); here we present the first report of this genus for Peru based in a specimen caught in a pitfall trap (Figure 3).

Our specimen was identified as Cryptonanus by the following combination of characters: small size, prehensile tail longer than head-and-body (Table 2), dorsal surface of tail covered by tiny sows, plantar surface of manus with distinct plantar pads, manual digits III and IV subequal in length (Voss et al., 2005). Nasals distinctly wider posteriorly than anteriorly, secondary foramen ovale absent, petrosal exposed on poster lateral surface of braincase through fenestra in parietal-squamosal suture, P3 taller than P2, unworn C1 with small accessory worn-out cusps (Figure 4). All this characters agreed with the description of this genus (Voss et al., 2005; Voss com. pers.). Furthermore, our specimen can be identified as C. unduaviensis by the following combination of characters: tail length more than 111 mm (Table 2), condylobasal length more than 25.5 mm, maxillary too throw more than 10.0 mm, length of upper molar series (M1-M4) more than 5.5 mm; venter self-colored light yellowish buff. The characters and measurements of our specimen fell within the range of variation described for C. unduaviensis in the literature (Voss et al., 2005; Gardner, 2007b; Voss & Jansa, 2009; Voss, com. pers.).

Left to right, dorsal, ventral and lateral views of cranium and mandible. (A) 
 Cryptonanus unduaviensis MUSA 12695; (B) 
 Rhogeessa hussoni MUSA 12902; and (C) and Rhogeessa io MUSA 12903. Scale bar equal to 10 mm.
FIGURE 4:: Left to right, dorsal, ventral and lateral views of cranium and mandible. (A) Cryptonanus unduaviensis MUSA 12695; (B) Rhogeessa hussoni MUSA 12902; and (C) and Rhogeessa io MUSA 12903. Scale bar equal to 10 mm.

Habitat:Voss et al. (2005) reported that one individual of C. unduaviensis was collected on a tree island surrounded by seasonally flooded grassland and another was in grass at the edge of a marshy stream. Our specimen was caught in the ecotone of the Aguas Claras Camp, on the sixth day that the pitfall traps line was working. Others small mammals caught in the same trap lines are Marmosops bishop, Neacomys minutus, and Necromys lenguarum.

Distribution: The specimen MUSA 12695 extends the distribution range of C. unduaviensis southwest from Independence, Pando (Bolivia) by 223 km (Anderson, 1997).

ORDER CHIROPTERA Blumenbach 1779

Family Vespertilionidae Gray 1821

Rhogeessa hussoni Genoways & Baker 1996

Husson’s Yellow Bat

Specimen examined: adult male (MUSA 12902), collected at Aguas Claras Camp, Pampas del Heath, Madre de Dios (12°57’20”S, 68°54’46”W, 216 m). Measurements see Table 3.

TABLE 3::
Measurements (mm) and weights (g) of the specimens of Rhogeessa hussoni and R. io from Peru compare with referred material of the genus Rhogeessa in South America (data from Goodwin, 1958; Ruedas & Bickman, 1992; Genoways & Baker, 1996; Aires et al., 2011). Holotype is denoted with asterisk and numbers in brackets include ranges.
    Rhogeessa hussoni     Rhogeessa io  
Measures Suriname Brasil Peru Venezuela   Peru
  * n = 4 MUSA 12902 * n = 10 MUSA 12903
Total length - - 81 - - 70
Tail length - - 31 - - 30
Hind foot length - (5.02 - 6.43) 6.1 - - 6.3
Ear length - (8.07 - 11.84) 12.5 - - 11.6
Forearm 30.2 (28.8 - 30.91) 28.6 28 - 28.8
3rd digit metacarpal 29 (26.3 - 28.2) 28.5 - (26.2 - 28.4) 26.8
4th digit metacarpal 27.8 - 28.1 - (25.9 - 27.4) 26.4
Greatest length of the skull 13.2 (12.6 - 13.2) 13.2 12.1 (11.7 - 12.6) 12.5
Condylobasal length 10 - 11.1 s/m (8.5 - 9.1) 10.6
Mastoid width 7.1 - 7.3 7+ - s/m
Breadth of braincase 5.7 - 6.2 6 - 6.1
Zygomatic width 8.9 - 8.9 8.1 - 8.3
Postorbital width 3.2 (3.41 - 3.80) 3.4 - - 3.2
Width across upper canines 3.8 (3.78 - 4.09) 3.9 - (3.4 - 3.6) 3.6
Width across second upper molars 5.6 - 5.7 5.5 (5.0 - 5.4) 5.6
Maxillary toothrow 4.7 (4.56 - 4.89) 4.9 4.6 - 4.8
Postpalatal length 4.7 - 4.9 - (4.0 - 4.4) 4.8
Mandibular toothrow 5.2 (5.06 - 5.34) 5.6 - (5.4 - 5.7) 5.4
Width across lower canines - (2.56 - 2.78) 2.8 - - 2.6

Remarks: The genus Rhogeessa is endemic to the Neotropical region and one group in that genus exhibits high species diversity despite a lack of morphological differentiation. The previously known complex of species named as R. tumida consists of five species (R. aeneus, R. genowaysi, R. io, R. velilla, and R. hussoni), which are distributed in Middle America and north of South America (Audet et al., 1993; Baird et al., 2008; 2012).

Genoways & Baker (1996) described R. hussoni based on one specimen from Sipaliwini Airstrip, District of Nickerie (Suriname), and included other report from Maranhão (Brazil). Years afterwards, Aires et al. (2011) presented new locality records extending the west distribution extension in Brazil (Nova Lacerda, Mato Grosso). Here we present the first report of this species for Peru based on a specimen caught in a mist net installed at ground level in open savanna (Figure 3).

Our specimen is identified as Rhogeessa hussoni due to following combination of characters: one upper and three lower incisors on each side; space between upper incisors narrow; one upper premolar on each side; upper surface of uropatagium not densely furred; dorsal and ventral coloration golden brown with brown tips; pads inflated above the muzzle (Figure 3). Forearm greater than 27.1 mm. Parietals not inflated at juncture of the sagittal crest with the lambdoidal crests (helmet lacking) (Figure 4); greatest length of skull more than 12.6 mm; width across first upper canines more than 3.7 mm (Table 3). All this characters agreed with the description of R. hussoni (Genoways & Baker, 1996; Bickham & Ruedas, 2007; Aires et al., 2011), however it necessary carry out citogenetic and molecular studies to confirm that (Backer, com. pers.).

Habitat: Rhogeessa hussoni has been found in mixed savanna, gallery forest, lowland evergreen rainforest and Atlantic Forest (Genoways & Baker, 1996; Aires et al., 2011). Our specimen was caught in the open savanna of Refugio Juliaca, the first night that the mist net was set. Others bats species caught in the same net were Artibeus lituratus, Carollia perspicillata and Noctilio albiventris.

Distribution: Our specimen MUSA 12902 extends the distribution range of R. hussoni in 1,031 km westwards from Córrego Areia Branca, Nova Lacerda, Brazil (Aires et al., 2011).

Rhogeessa io Thomas 1903

Thomas’s Yellow Bat

Specimen examined: sub-adult male (MUSA 12903), collected at Aguas Claras Camp, Pampas del Heath, Madre de Dios (12°57’20”S, 68°54’46”W, 216 m). Measures see Table 3.

Remarks:Pacheco et al. (2007) were the first to report Rhogeessa in Peru, the species R. io, based in specimens from northwest Peru (Zarumilla, Tumbes), however Pacheco et al. (2009), following Baird et al. (2008, 2009), tentatively assign that samples as R. velilla and therefore R. io was not considered in the last list of mammals of Peru. Nevertheless, here we present the first report of R. io for Peru based on a specimen caught in a mist net installed 2 m above level ground in the ecotone.

MUSA 12903 was identified as Rhogeessa io by the following character combinations: one upper and three lower incisors on each side; space between upper incisors narrow; one upper premolar on each side; upper surface of uropatagium not densely furred; dorsal coloration light brown and ventral coloration pale yellow; pads inconspicuous above the muzzle. Forearm greater than 27.1 mm. Parietals not inflated at juncture of the sagittal crest with the lambdoidal crests (helmet lacking) (Figure 4); greatest length of skull less than 12.6 mm; width across first upper canines less than 3.7 mm (Table 3). All this characters agreed with the description of R. io (Thomas, 1903; Bickham & Ruedas, 2007; Aires et al., 2011), however it necessary carry out citogenetic and molecular studies for confirm that (Backer, com. pers.).

Habitat: Rhogeessa io is the most widely distributed Rhogeessa in South America and it inhabits a variety of habitats, including evergreen and deciduous forest, thorn shrub, open areas, and villages (Bickham & Ruedas, 2007; Soriano & Tavares, 2008). Our specimen was caught in the ecotone of Refugio Juliaca, in the second night that the mist net was set. Others bats species caught in the same net were Artibeus lituratus, Artibeus obscurus, Carollia brevicauda, Carollia perspicillata, Uroderma bilobatum, and Vampyriscus bidens.

Distribution: The specimen MUSA 12903 extends the distribution range of R. io 444 km westward from Caravana, Beni, Bolivia (Bickham & Ruedas, 2007).

Our results suggest the existence of at least 111 species of mammals in Pampas del Heath and surrounding habitats, resulting number of the 69 species recorded here, 74 documented by Emmons et al. (1994) and 72 listed by Luna et al. (2002). However, due to isolated location of Pampas del Heath from rest of Cerrado, it possible that several forms of small mammals reported here (e.g., Lutreolina crassicaudata, Cerradomys maracajuensis or Pseudoryzomys simplex) could be different afterward taxonomic studies more detailed (molecular analyzes).

Others small mammals species that could be potentially registered in the Pampas del Heath and surrounding are Kunsia tomentosus, Caluromysiops irrupta, Marmosa rubra, Marmosa (Micoureus) demerarae, Metachirus nudicaudatus, Holochilus sciureus, Juscelinomys sp., Diclidurus albus, Peropteryx kappleri, Saccopteryx leptura, S. canescens, Desmodus rotundus, Diphylla ecaudata, Micronycteris minuta, Phylloderma stenops, Artibeus anderseni, Vampyrum spectrum, Sphaeronycteris toxophyllum, Noctilio leporinus, Pteronotus parnelli, and Myotis simus. Because of they have been recorded Protected Areas near to Pampas del Heath, or are commonly caught in the Bolivian’s savanna (Emmons et al., 2002; Emmons et al., 2006a; 2006b; Solari et al., 2006; Terán et al., 2008; Emmons & Patton, 2012).

Our new records for Peru add one more genus and three species to the country reaching to 541 mammal species in Peru (Pacheco et al., 2009; Lim et al., 2010; Velazco et al., 2010a, 2010b; Gregorin & Almeida, 2010; Gutiérrez et al., 2010; Mantilla-Meluk & Baker, 2010; Díaz, 2011; Velazco & Cadenillas, 2011; Hice & Velazco, 2012; Larsen et al., 2012; Medina et al., 2012; Jiménez et al., 2013; Marsh, 2014; Medina et al., 2014; Pacheco et al., 2014; Rengifo et al., 2014; Velazco et al., 2014; Zeballos et al., 2014; Patton et al., 2015; Hurtado & Pacheco, 2015; Vermeer & Tello-Alvarado, 2015). That show the importance of conduced Flora and Fauna Monitoring Programs for knowing better the diversity of Peruvian mammals in Peru as a whole and in Pampas del Heath in particular.

Sampling effort

Graphs of the species accumulation of small mammals built with the observed data show a trend of increasing richness species if it rises the sampling effort in each of the vegetation forms studied (Figure 5), suggesting that not overall species richness was registered.

Species accumulation curves for each vegetation types evaluated. Empirical curves (upper left) and Clench models (the rest).

FIGURE 5:: Species accumulation curves for each vegetation types evaluated. Empirical curves (upper left) and Clench models (the rest).

Clench models obtained for the savanna, ecotonal area and forest had a good adjust with R2 values of 0.9992, 0.9993 and 0.9997, respectively. The model estimated a total of 45 species for the savanna, 53 for the ecotonal area and 49 for the forest (Figure 4), but in neither case is the asymptote reached (pending 1.52 in savanna, 1.65 in ecotonal area and 1.52 in forest). Moreover, the model indicates that 61% of total species have been registered during our assessment in the Savanna, while in the ecotone and forest have been 53% and 51%, respectively. The model estimated that 17, 28.9 and 29.8 days (sampling events) of assessment would be capable of recording the 80% of predicted species in the savanna, ecotonal area and forest (respectively), while Aguirre (2002) estimated 30 nigths of sampling effort for to register the 88% of bats species in Bolivian’s savanna.

Relative density

The marsupial Marmosops bishopi, the rodent Necromys lenguarum, and the bats Artibeus lituratus and A. planirostris were the most abundant during the survey. Less abundant species were usually represented by a single individual: the marsupials Cryptonanus unduavensis, Lutreolina crassicaudata, Marmosa lepida, M. (Micoureus) regina and Marmosops noctivagus; the rodents Oligoryzomys microtis, Oligoryzomys sp.; and the bats Myotis riparius, Platyrrhinus incarum, Rhogeessa hussoni, R. io, and Trachops cirrhosus (Table 1).

In the savanna, only two species of marsupials were reported and this were equally abundant (Marmosops sp. and Lutreolina crassicaudata). The most abundant rodents were Necromys lenguarum and Pseudoryzomys simplex, meanwhile in the bats were Artibeus lituratus and Myotis nigricans (Table 1). Respect to the bats, our relative densities in the savanna are similar to the surveys in Noel Kempff Mercado National Park and Espiritu’s savanna, when frugivores bats (Carollia spp. and Artibeus lituratus) and slow-flying insectivores bats (Myotis nigricans and Noctilio albiventris) were the most commons, respectively (Aguirre, 2002; Emmons et al., 2006b).

In the ecotonal area, the marsupial Monodelphis peruviana, the rodents Euryoryzomys nitidus and Hylaeamys perenensis, and the bats Glossophaga soricina and Carollia perspicillata were the most abundant species, meanwhile in the forest were the marsupial M. bishopi, the rodents H. perenensis and E. nitidus, and the bats Artibeus gnomus, A. lituratus, Artibeus obscurus and A. planirostris (Table 1).

There were species occupying the three vegetation forms but these have fluctuation in their densities surely as response to the environments resources in each vegetation form (Mohammadi, 2010). Thus, we found some species more abundant in forest environments (e.g., Marmosops sp., E. nitidus, H. perenensis and A. gnomus) than in open environments (e.g., Uroderma bilobatum and A. lituratus), and vice versa (Table 1).

Diversity

The diversity of marsupial and rodents in the ecotonal area (DMg = 3.53 and DMn = 2.26) and forest (2.49 and 1.64) were upper than savanna (1.26 and 0.91), however the diversity of bats was similar between the Savanna (3.52 and 2.51), Ecotonal area (3.51 and 2.50) and Forest (3.53 and 2.52).

These fluctuations could be explained since several approaches (resource foods, refuges, temperature, between others) nevertheless we suspect of the influence of moonlight on behavior of the marsupials and rodents, due to during the survey in the savanna the moon was in waxing crescent (November 31), likewise in the ecotonal area and forest that was full (December 10) to waning gibbous (December 14) (US Naval Oceanography, 2012). Effect of moonlight has been well documented for several nocturnal mammals by reducing their use of open space, or restricting their activity to darker periods of the night (Morrison, 1978; Gilbert & Boutin, 1991; Wolfe & Summerlin, 1989; Upham, 2008).

Community structure

Savanna’s range-abundance curves showed bats assemblages dominated by two species, one frugivorous and other insectivorous, being remarkable the presence of a greater number of insectivores species (1 sp.) compared with the rest of trophic groups (eight sp., frugivorous and nectarivorous). On the other hand the marsupials and rodents assemblages showed a wide variety of trophic groups, which were greatly dominated by insectivorous species (Figure 6). Both curves resemble the Fishers’s logarithmic series model (Fisher et al., 1943), which describes a community dominated by one or two species very abundant followed by many with lower abundances. This model generally applies to small communities under stress or pioneers, where one or a few factors dominate the ecology of the community (Moreno, 2001; Magurran, 1988).

Range-abundance curves (pi) for small mammals from Pampas del Heath. Codes of each species are denoted in Table 1. Trophic group: Insectivorous (full triangles), Frugivorous (circles), Herbivorous (empty circles), Carnivorous (stars), Omnivorous (empty triangles), Nectarivorous (diamonds) and Granivorous species (squares).

FIGURE 6:: Range-abundance curves (pi) for small mammals from Pampas del Heath. Codes of each species are denoted in Table 1. Trophic group: Insectivorous (full triangles), Frugivorous (circles), Herbivorous (empty circles), Carnivorous (stars), Omnivorous (empty triangles), Nectarivorous (diamonds) and Granivorous species (squares).

Ecotone’s range-abundance curves showed a bats assemblages dominated by frugivorous species, followed by some insectivorous and nectarivorous species. Whereas for the marsupials and rodents community showed a wide variety of trophic groups, whose species had similar abundances (Figure 6).

Forest’s range-abundance curves showed a bats assemblages dominated by two species, one nectarivorous and other frugivorous, with the presence of a greater number of frugivorous species (nine sp.) compare with the rest of trophic groups. Whereas the marsupials and rodents assemblages showed a slight dominance by frugivorous species and there was a greater richness of insectivorous species (six species) compared with the other trophic groups (four species, frugivorous and granivorous) (Figure 6).

Curves constructed for the ecotonal area and forest seem fit to a Log normal distribution model (Sugihara, 1980), which describe communities with light equilibria between number of the most abundant species and least abundant species. This model generally characterize samples of large, mature and diverse communities due to there is a hierarchical segregation of niche used by the organisms (Moreno, 2001; Magurran, 1988).

Emmons et al. (1994) and Luna et al. (2002) reported a high richness of insectivorous bat species in Pampas del Heath, however it is notable replacement of organisms between the savanna, ecotonal area and forest. Our data showed a great dominance of insectivorous species in open habitats, like savanna, which are gradually replaced by frugivorous species conform the vegetation change forward arboreal habitats, like ecotonal area and forest (Figure 6).

Conservation status

Thirteen species are categorize as threatened according to Peruvian and international law, which two are in Data insufficient (IUCN, 2012; MINAGRI, 2014). Additionally 24 suffer pressure of International Trade (CITES, 2013), which seven are categorized on Appendice I, 15 on Appendice II and two on Appendice III (Table 4).

Table 4::
Conservation status of mammals registered during the study.
Species Accounts   Conservation status   Endemic from Savanna
  DS 04-2014 IUCN CITES  
DIDELPHIMORPHIA        
Cryptonanus unduaviensis       X
Lutreolina crassicaudata       X
CINGULATA        
Priodontes maximus VU VU I  
PILOSA        
Myrmecophaga tridactyla VU   II  
PRIMATES        
Cebus albifrons     II  
Saguinus fuscicollis     II  
Saguinus imperator     II  
Aotus azarae     II  
Saimiri sciureus     II  
Sapajus apella     II  
Callicebus sp.     II  
Alouatta sara     II  
Ateles chamek EN EN II  
RODENTIA        
Cerradomys maracajuensis       X
Pseudoryzomys simplex       X
Oligoryzomys sp.       X
Dinomys branickii VU VU    
Cavia aperea       X
CARNIVORA        
Leopardus pardalis     I  
Leopardus wiedii DD   I  
Panthera onca NT   I  
Puma concolor NT   II  
Atelocynus microtis VU      
Chrysocyon brachyurus     II X
Eira barbara     III  
Lontra longicaudis     I  
Pteronura brasiliensis EN EN I  
Potos flavus     III  
PERISSODACTYLA        
Tapirus terrestris NT VU II  
ARTIODACTYLA        
Pecari tajacu     II  
Tayassu pecari NT VU II  
Blastocerus dichotomus VU VU I X
Mazama americana DD      
Total species 13 7 24 8

Eight species corresponding to endemic mammals from Neotropical savannas (Table 4) (Emmons et al., 1994; Luna et al., 2002; Voss et al., 2005; Emmons et al., 2002; 2006a; 2006b; Percequillo et al., 2008).

Future studies that may be interesting to Pampas del Heath are the dynamic between particular vegetation of the savanna and mammal with the skilled of modifying that such as Cavia aperea and Blastocerus dichotomus (herbivorous species), or studies about population status of carnivorous species (Lutreolina crassicaudata and Chrysocyon brachyurus).

Acknowledgements

ACKNOWLEDGEMENTS

We are grateful to U.F. Pardiñas (Centro Nacional Patagónico), B.D. Patterson (Field Museum of Natural History) and J. Salazar-Bravo (Museum of Natural History, Texas Tech University) for suggestions that improved an earlier version of the manuscript. Finally R. Gutiérrez and D. Huamán for fieldwork support. This study was supported by Asociación para la Investigación y Desarrollo (AIDER), Museo de Historia Natural de la Universidad Nacional de San Agustín de Arequipa (MUSA) and Bahuaja Sonene National Park, which it had the help of Wildlife Conservation Society (WCS). We also thanks the Ministerio de Ambiente and SERNANP for the permits to capture and collect specimens (RJ 007-2011).

REFERENCES

  1. (). Structure of a neotropical savanna bat community. Journal of Mammalogy 83, 775-784.
  2. , , (). Mammalia, Chiroptera, Vespertilionidae, Rhogeessa hussoni Genoways & Baker, 1996: Distribution extension and taxonomic notes. Checklist 7, 117-119.
  3. (). Mammals of Bolivia, taxonomy and distribution. Bulletin of the American Museum of Natural History 231, 1-652.
  4. , , , , (). . . Canberra: CSIRO. . ACIAR Monograph, n. 100
  5. , , (). Morphology, karyology, and echolocation calls of Rhogeessa (Chiroptera: Vespertilionidae) from the Yucatan Peninsula. Journal of Mammalogy 74, 498-502.
  6. , , , (). Evolutionary history of the genus Rhogeessa (Chiroptera: Vespertilionidae) as revealed by mitochondrial DNA sequences. Journal of Mammalogy 89, 744-754.
  7. , , , (). Speciation by monobrachial centric fusions: A test of the model using nuclear DNA sequences from the bat genus Rhogeessa. Molecular Phylogenetics and Evolution 50, 256-267.
  8. , , , (). Morphological analysis and description of two new species of Rhogeessa (Chiroptera: Vespertilionidae) from the Neotropics. Occasional Papers of the Museum of Texas Tech University 281, 1-25.
  9. , (). . , ed. . Chicago: University of Chicago Press. 1., 483-484.
  10. , (). . . Washington: U.S. Department of Health Education and Welfare. . Public Health Monograph, 55
  11. (). . . . Appendices I, II y IIIAvailable in: www.iucnredlist.org (accessed )
  12. , (). . . Plymouth, UK: Primer-E Ltd. . User Manual/Tutorial
  13. (). New records of bats from the northern region of the Peruvian Amazon. Zoological Research 32, 168-178.
  14. (). El Uso de Entrevistas para averiguar la distribución de Vertebrados. Revista de Ecología Latinoamericana 2, 1-4.
  15. , (). . . Chicago: The University of Chicago Press. .
  16. , (). . . Santa Cruz de la Sierra: Editorial F.A.N.. .
  17. , (). Taxonomic revision of Bolivian Juscelinomys (Rodentia, Cricetidae) with notes on morphology and ecology. Mammalia 76, 285-294.
  18. , , (). . , , , eds. . Washington: Conservation International. .146-149. RAP Working Papers 6
  19. , , , , , , (). The non-flying mammals of Noel Kempff Mercado National Park (Bolivia). Revista Boliviana de Ecología 19, 23-46.
  20. , , , , (). . , ed. . Washington: Conservation International. .106-110. RAP Working Papers 24
  21. , , , , , (). The forest and savanna bat communities of Noel Kempff Mercado National Park (Bolivia). Revista Boliviana de Ecología 19, 47-57.
  22. (). . . Washington: Island Press. .
  23. , , (). The relation between the number of species and the number of individuals in a random sample of animal population. Journal of Animal Ecology 12, 42-58.
  24. (). . . University of Chicago, Chicago Press. .
  25. (). . , ed. . University of Chicago, Chicago Press. .40-43.
  26. , (). . , , eds. . Lubbock: Museum of Texas Tech University. 1., 83-87.
  27. , (). Effect of moonlight on winter activity of snowshoe hares. Arctic and Alpine Research 23, 61-65.
  28. (). Bats of the genus Rhogeessa. American Museum Novitates 1923, 1-17.
  29. , (). . . Ulm: Reta Verlag. 1.
  30. (). A simple ground-based method for trapping small mammals in the forest canopy. Mastozoología Neotropical 10, 177-181.
  31. , (). Revalidation of Promops davisoni Thomas (Molossidae). Chiroptera Neotropical 16, 648-659.
  32. , (). Role of diet selection in the use of habitat by pampas cavies Cavia aperea pamparum (Mammalia, Rodentia). Mammalia 62(1), 23-36.
  33. , , (). Molecular systematics of mouse opossums (Didelphidae: Marmosa): assessing species limits using mitochondrial DNA sequences, with comments on phylogenetic relationships and biogeography. American Museum Novitates 3692, 1-22.
  34. , (). Biogeographie der Beni-savannen (Bolivien). Geographische Rundschau 48, 662-668.
  35. , (). The Non-volant Mammals of the Reserva Nacional Allpahuayo-Mishana, Loreto, Peru. Special Publications 60, 1-135.
  36. , , (). Bats of the Reserva Nacional Allpahuayo-Mishana, northeastern Peru, with notes on community structure. Acta Chiropterologica 6, 319-334.
  37. , , (). Registro de dos nuevos mamíferos para el Perú, Odocoileus dichotomus (Illiger-1811) y Chrysocyon brachyurus (Illiger-1811) con notas sobre su hábitat. Revista Forestal del Perú 6, 61-81.
  38. , (). New mammalian records in the Parque Nacional Cerros de Amotape, northwestern Peru. Revista Peruana de Biología 22(1), 77-86.
  39. , , , (). . , , eds. . Santa Cruz de la Sierra: Editorial FAN. 1., 47-88.
  40. (). . , ed. . . Version 2012.1Available in: www.iucnredlist.org (accessed )
  41. , , (). An introduction to the systematics of Akodon orophilus Osgood, 1913 (Rodentia: Cricetidae) with the description of a new species. Zootaxa 3669, 223-242.
  42. , (). Las curvas de acumulación de especies y la necesidad de evaluar la calidad de los inventarios biológicos. Revista Ibérica de Aracnología 8, 151-161.
  43. , , , (). . , , , , , eds. . Washington: Smithsonian Institution Press. 1., 115-155.
  44. , , , , , , , , , , , , , , , , , , (). . . Arlington: NatureServe. .
  45. , , , , , , (). Genetic diversity of neotropical Myotis (Chiroptera: Vespertilionidae) with an Emphasis on South American Species. PLoS ONE 7
  46. (). Systematics of the genus Rhogeessa (Chiroptera: Vespertilionidae). Occasional Papers of the Museum of Natural History the University of Kansas 19, 1-47.
  47. , , (). . . Chicago: Asociación para la Conservación de la Cuenca amazónica (ACCA) y Environmental & Conservation Programs, The Field Museum. .
  48. , , , , , (). A New Species of Peropteryx (Chiroptera: Emballonuridae) from Western Amazonia with Comments on Phylogenetic Relationships within the Genus. American Museum Novitates 3686, 1-20.
  49. , , , (). . . Arequipa: Universidad Nacional de San Agustín. .
  50. , , , (). . , ed. . Washington: Conservation International. 1., 66-70. Bulletin of Biological Assessment 24
  51. (). . . New Jersey: Princeton University Press. .
  52. , (). New species of Anoura (Chiroptera: Phyllostomidae) from Colombia, with systematic remarks and notes on the distribution of the A. geoffroyi complex. Occasional Papers of the Museum of Texas Tech University 292, 1-18.
  53. (). A taxonomic revision of the Saki Monkeys, Pithecia Desmarest, 1804. Neotropical Primates 21, 1-163.
  54. , , , , (). A new species of Eumops (Chiroptera: Molossidae) from southwestern Peru. Zootaxa 3878, 19-36.
  55. , , , , , (). Primer registro de Eumops patagonicus y ampliación del rango de distribución geográfica de E. hansae, en el sur de Perú. Mastozoología Neotropical 19, 345-351.
  56. (). Actualización de la lista de Clasificación y Categorización de Especies Amenazadas de Fauna Silvestre legalmente protegidas por el Estado. El Peruano: Decreto Supremo 1(004-2014), 520497-520504.
  57. (). . . Lima: Editorial Super Gráfica EIRL. .
  58. (). Microhabitat Selection by Small Mammals. Advances in Biological Research 4, 283-287.
  59. (). . . Zaragoza: M&T. 1. Manuales y Tesis SEA
  60. (). Lunar phobia in a neotropical fruit bat, Artibeus jamaicensis (Chiroptera, Phyllostomidae). Animal Behaviour 26, 852-855.
  61. Ecologia alimentar de pequenos mamíferos de áreas de Cerrado no Sudeste do Brasil Dissertação de Mestrado thesis
  62. , , (). Noteworthy bat records from the Pacific Tropical rainforest region and adjacent dry forest in northwestern Peru. Acta Chiropterologica 9(2), 409-422.
  63. , , , , (). Diversidad y endemismo de los Mamíferos del Perú. Revista Peruana de Biología 16, 5-32.
  64. , , (). Una nueva especie de ratón orejón del género Phyllotis Waterhouse, 1837 (Rodentia: Cricetidae) del norte del Perú. Therya 5(2), 481-508.
  65. , , (). Mammals of the Rio Juruá and the evolutionary and ecological diversification of Amazonia. Bulletin of the American Museum of Natural History 244, 1-306.
  66. , , (). . . Chicago: The University of Chicago Press. .
  67. , , (). Systematic review of genus Cerradomys Weksler, Percequillo and Voss, 2006 (Rodentia: Cricetidae: Sigmodontinae: Oryzomyini), with description of two new species from Eastern Brazil. American Museum Novitates 3622, 1-46.
  68. , (). Taxonomic revision of the Andean leaf-eared mouse, Phyllotis andium Thomas 1912 (Rodentia: Cricetidae), with the description of a new species. Zootaxa 4018(3), 349-380.
  69. , (). Morphological differentiation between Rhogeessa minutilla and R. tumida (Mammalia: Chiroptera: Vespertilionidae). Proceedings of the Biological Society of Washington 105, 403409.
  70. , (). The use of species accumulation functions for the prediction of species richness. Conservation Biology 7, 480-488.
  71. , , , , (). Mammals of the Manu Biosphere Reserve. Fieldiana: Zoology N.S. 110, 13-23.B.D Patterson.; D.F. Stotz & S. Solari, (Eds.). Mammals and Birds of the Manu Biosphere Reserve, Peru
  72. , , (). . . . Available in: www.iucnredlist.org (accessed )
  73. (). . . Tulsa, OK: StatSoft, Inc.. .
  74. (). Minimal community structure: an explanation of species abundance patterns. The American Naturalist 116, 770-787.
  75. (). Brief diagnoses of twenty-six apparently new forms of Marmosa (Marsupialia) from South America. American Museum Novitates 493, 1-14.
  76. , , (). Primer registro de Kunsia tomentosus (Rodentia: Cricetidae: Sigmodontinae) en el norte del departamento de La Paz, Bolivia. Mastozoología Neotropical 15, 129-133.
  77. (). Two South American forms of Rhogeessa. Annals and Magazine of Natural History 7, 382-383.
  78. Rodent activity in relation to moonlight in sandy and open habitats of the great basin desert Ms Thesis thesis
  79. (). . Phases of the Moon and Percent of the Moon Illuminated. Available in: www.usno.navy.mil/USNO/astronomical-applications/data-services (accessed )
  80. , (). On the identity of Lophostoma silvicolum occidentalis (Davis & Carter, 1978) (Chiroptera: Phyllostomidae). Zootaxa 2962, 1-20.
  81. , , (). Systematics of the Platyrrhinus helleri species complex (Chiroptera: Phyllostomidae), with descriptions of two new species. Zoological Journal of the Linnean Society 159, 785-812.
  82. , , , (). Extraordinary Local Diversity of Disk-Winged Bats (Thyropteridae: Thyroptera) in Northeastern Peru, with the Description of a New Species and Comments on Roosting Behavior. American Museum Novitates 3795, 1-28.
  83. , , (). First occurrence of the rare emballonurid bat Cyttarops alecto (Thomas, 1913) in Peru - Only hard to find or truly rare?. Mammalian Biology 76, 373-376.
  84. , (). The Distribution and Taxonomy of Titi Monkeys (Callicebus) in Central and Southern Peru, with the Description of a New Species. Primate Conservation 29, 9-29.
  85. , (). Mammalian diversity in neotropical lowland rainforests: a preliminary assessment. Bulletin of the American Museum of Natural History 230, 1-115.
  86. , (). Phylogenetic relationships and classification of Didelphidae marsupials, an extant radiation of New World metatherian mammals. Bulletin of the American Museum of Natural History 322, 1-177.
  87. , , (). On the contents of Gracilinanus Gardner & Creighton, 1989, with the description of a previously unrecognized clade of small didelphid marsupials. American Museum Novitates 3482, 1-34.
  88. , , (). The Mammals of Paracou, French Guiana: A Neotropical lowland rainforest fauna. Part 2. Nonvolant species. Bulletin of the American Museum of Natural History 263, 1-236.
  89. , (). Key to the genera of the tribe Oryzomyini (Rodentia: Cricetidae: Sigmodontinae). Mastozoología Neotropical 18, 281-292.
  90. , (). The influence of lunar light on nocturnal activity of the old field mouse. Animal Behavior 37, 410-414.
  91. , , , (). Phylogenetic relationships of Calomys sorellus complex (Rodentia: Cricetidae), with the description of two new species. Revista Mexicana de Mastozoología Nueva Época 4, 1-23.

Publicado com o apoio financeiro do Programa de Apoio às Publicações Científicas Periódicas da USP