Rhogeessa H. Allen 1866

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.

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 assemblagesdominated bytwo species, onefrugivorous 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).

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).

Eightspecies corresponding toendemic 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 Chrysocyonbrachyurus).