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Acta Chiropterologica, 9(2): 535–546, 2007

PL ISSN 1508-1109 © Museum and Institute of Zoology PAS

Feeding habits of Noctilio albiventris (Noctilionidae) bats in the Pantanal, Brazil FERNANDO GONÇALVES1, ROBERTO MUNIN1 ,2, PRISCILA COSTA1, and ERICH FISCHER1, 3
de Biologia, Universidade Federal de Mato Grosso do Sul, 79070-900 Campo Grande, Mato Grosso do Sul, Brasil 2 Programa de Pós-Graduaçno em Ecologia e Conservaçao, Universidade Federal de Mato Grosso do Sul, 79070-900 Campo Grande, Mato Grosso do Sul, Brasil 3 Corresponding author: E-mail: Key words: bulldog bats, Noctilio, diet, frugivory, insectivory, wetlands

INTRODUCTION The lesser bulldog bat, Noctilio albiventris, and the greater bulldog bat, N. leporinus (Noctilionidae) occur from Mexico to Argentina and Uruguay and are known to forage over water courses and ponds (Hood and Pitocchelli, 1983; Hood and Jones, 1984; Fenton et al., 1993; Kalko et al., 1998; Nogueira and Pol, 1998). Noctilio albiventris (20–40 g) feeds mainly on insects whereas N. leporinus (45–90 g) primarily eats fish, but both species are able to feed on insects and fish (Howell and Burch, 1974; Hood and Pitocchelli, 1983; Hood and Jones, 1984; Lewis-Oritt et al., 2001; Bordignon, 2006). Noctilio albiventris often captures insects in the air but notably gleans them from water surfaces (Kalko et al., 1998; Nogueira and Pol, 1998). Compared to other Neotropical insectivorous bats, N. albiventris prey upon a wider variety of insect orders and a wider range of prey size (Aguirre et al., 2003). Although most available data do not indicate herbivory

for N. albiventris, seeds of Brosimum and Morus (Moraceae) and pollen of Ceiba (Bombacaceae) have been recorded in their faeces or stomachs (Howell and Burch, 1974). Data on N. albiventris feeding habits, however, are very scarce and limited to Central America and only Bolivia in South America (Hooper and Brown, 1968; Howell and Burch, 1974; Whitaker and Findley, 1980; Aguirre et al., 2003). Here, we studied food items recorded from faecal samples of N. albiventris in three sites in the Pantanal wetlands in Brazil. We describe orders of insects, and plant species (seeds and pollen) consumed by this bat. MATERIALS AND METHODS
The Pantanal floodplain (ca. 160,000 km2) is markedly seasonal, with a dry period from April to September and a wet period from October to March. Vegetation is composed of forest patches intermixed with seasonally flooded grasslands (Prance and Schaller, 1982; Araujo and Sazima, 2003). Noctilio albiventris individuals were mist-netted in forest patches during 47 field expeditions from May 1998 to April 2007, at three sites: Rio Negro farm (19°34’S,


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56°14’W) (20 expeditions), Nhumirim farm (18°59’S, 56°37’W) (seven expeditions), and Passo do Lontra village (19°34’S, 57°02’W) (20 expeditions). In three to four nights per expedition, six to 10 mist-nets (12 × 2.6 m) were opened between 18:00 and 00:00 hr. Captured bats were kept in cloth bags for 45 to 60 min to obtain faecal samples. Cloth bags were used only once during each field expedition and washed between expeditions. Each faecal sample was individually placed in hermetically sealed plastic tubes and stored immersed in glycerine. In the laboratory, samples were inspected under a stereomicroscope to register the presence of seeds, pollen and arthropod parts. Nevertheless, we did not inspect three faecal samples from Rio Negro or any from Passo do Lontra for arthropods and pollen. Species of seeds and pollen were identified by comparison with material collected from plants at the study sites and from the CGMS Herbarium. Insect parts were classified into orders based on literature. Bat voucher specimens were deposited in the ZUFMS collection.

RESULTS We captured 125 N. albiventris individuals, of which 77 supplied faecal samples. Twenty seven samples were from bats netted at Passo do Lontra, 25 from Nhumirim and 25 from Rio Negro. The faecal samples presented five orders of insects, one spider, nine species of seeds and one species of pollen (Table 1). Arthropods occurred in all samples (n = 47) inspected; each faecal sample showed one to four orders of insects. Hemiptera and Coleoptera were the most frequent, accounting for 81 and 64% of the samples respectively (Table 1). There was no difference (G = 5.87, d.f. = 4, P = 0.21) in the proportion of insect orders between Rio Negro and Nhumirim sites.

TABLE 1. Number (and percentage) of N. albiventris (Noctilionidae) faecal samples containing different food items, at three sites in the Pantanal, Brazil, arranged in decreasing order of importance. Sample sizes are given in brackets Food items Hemiptera Coleoptera Lepidoptera Diptera Hymenoptera Araneae Unidentified ∑ Morphspecies 1 Cecropia pachystachya Ficus guaranitica Maclura tinctoria Ficus pertusa Ficus sp. Banara arguta Morphspecies 2 Morphspecies 3 ∑ Bauhinia ungulata
* **

Rio Negro [25]* 15 (68) 11 (50) 12 (54) 3 (14) 3 (14) 1 (5) 3 (14) 22 (100) 3 (12) 2 (8) 0 2 (8) 0 0 0 0 0 7 (28) 2 (9)

Sites Nhumirim [25] Passo do Lontra [27] Arthropods 23 (92) 19 (76) 8 (32) 8 (32) 1 (4) 0 1 (4) 25 (100) Seeds 6 (24) 0 2 (8) 0 0 0 1 (4) 1 (4) 1 (4) 8 (32) Pollen 0 – – – – – – – – 0 1 (4) 0 0 1 (4) 1 (4) 0 0 0 3 (11) –

Total [77]** 38 (81) 30 (64) 20 (43) 11 (23) 4 (9) 1 (2) 4 (9) 47 (100) 9 (12) 3 (5) 2 (3) 2 (3) 1 (2) 1 (2) 1 (2) 1 (2) 1 (2) 18 (23) 2 (4)

— Three faecal samples were not inspected for arthropods and pollen — Thirty faecal samples were not inspected for arthropods and pollen

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Seeds occurred in 18 samples (23%), and pollen (n > 50) of Bauhinia ungulata in two samples (4%). Morphspecies 1 was the most frequent seed (12%). Seeds of Banara arguta, Cecropia pachystachya, Ficus guaranitica, F. pertusa, Ficus sp., and Maclura tinctoria occurred in 2 to 5% of the samples. Each faecal sample presented one (n = 15) or two (n = 3) species of seeds and the number of seeds per faecal sample varied from 5 to 40. Cecropia pachystachya and the morphspecies 1 were found in faecal samples from two sites, while the other species of seeds were registered at only one site (Table 1). The proportion of samples containing seeds was similar between Rio Negro (7/25) and Nhumirim (8/25) sites, but it was lower at Passo do Lontra (3/27). DISCUSSION Available data indicate that N. albiventris is primarily, and sometimes exclusively, insectivorous (Hood and Pitocchelli, 1983). Occasional frugivory for N. albiventris has been weakly supported by records of seeds of Brosimum in four faecal samples and of seeds of Morus in ‘several’ N. albiventris stomachs (Howell and Burch, 1974). In the Pantanal, N. albiventris’ diet appears to partially rely on fruits since seeds constantly occurred throughout long-term sampling at different sites. Richness of seeds among the faecal samples was also unexpectedly high. Noctilio albiventris fed on nine species of fruits, of which at least seven, i.e. C. pachystachya, Ficus sp., F. guaranitica, F. pertusa, Banara arguta, and morphspecies 2 and 3, are shared with Phyllostomid bats at the study sites; only seeds of M. tinctoria and morphspecies 1 were not recorded in faeces from other Pantanal bat species (personal observations). However, Oprea et al. (2007) have reported M. tinctoria as food for Phyllostomids. Based on previous records and on the present study, occasional

frugivory by N. albiventris seems to be mainly associated with Moraceae species — Morus, Brosimum, Ficus and Maclura — whose fruits are typically consumed by frugivorous Phyllostomids. Insectivory by N. albiventris in the Pantanal was concentrated on Hemiptera, contrasting with the studies in Costa Rica and Bolivia where the most common prey were Coleoptera (Hooper and Brown, 1968; Whitaker and Findley, 1980; Aguirre et al., 2003). This relatively high frequency of hemipterans preyed on by N. albiventris in the Pantanal might be related to differences in the insect assemblages among regions. Pollen of B. ungulata (present study) and Ceiba sp. (Howell and Burch, 1974) might have been unintentionally ingested by N. albiventris individuals through predation on flower-visiting insects carrying pollen. Our samples that contained pollen also presented lepidopteran parts, an order which includes potential visitors of B. ungulata flowers (personal observations). Even so, the alternative hypothesis that N. albiventris individuals intentionally feed on pollen should not be discarded at all, as the recorded pollen species are from bat-pollinated flowers (Fischer, 1992; Gribel et al., 1999). Furthermore, in the Pantanal, two N. albiventris individuals were captured in front of open flowers of another bat-pollinated tree, Hymenaea stigonocarpa (R. Oliveira, personal communication). Additional studies on N. albiventris feeding habits in different regions are important to evaluate whether occasional herbivory is characteristic of the Pantanal populations or occurs widely in this species. ACKNOWLEDGEMENTS
To C. Santos, C. CorrLa, G. Graciolli, R. Teixeira, and S. Ferreira for valuable help in the field and laboratory; to L. Asborno, D. Hay, and T. Peters for English reviewing; and to anonymous referees for improvement of the manuscript. This study was


Short Notes HOOPER, E. T., and J. H. BROWN. 1968. Foraging and breeding in two sympatric species of Neotropical bats, genus Noctilio. Journal of Mammalogy, 49: 310–312. HOWELL, D. J., and D. BURCH. 1974. Food habits of some Costa Rican bats. Revista de Biologia Tropical, 21: 281–294. KALKO, E. K. V., H.-U. SCHNITZLER, I. KAIPF, and A. D. GRINNELL. 1998. Echolocation and foraging behavior of the lesser bulldog bat, Noctilio albiventris: preadaptations for piscivory. Behavioral Ecology and Sociobiology, 42: 305–319. LEWIS-ORITT, N., R. A. VAN DEN BUSSCHE, and R. J. BAKER. 2001. Molecular evidence for evolution of piscivory in Noctilio (Chiroptera: Noctilionidae). Journal of Mammalogy, 82: 748–759. NOGUEIRA, M. R., and A. POOL. 1998. Observaçtes sobre os hábitos de Rhynchonycteris naso (WiedNeuwied, 1820) e Noctilio albiventris Desmarest, 1818 (Mammallia, Chiroptera). Revista Brasileira Biologia, 58: 473–480. OPREA, M., D. BRITO, T. B. VIEIRA, P. MENDES, S. R. LOPES, R. M. FONSECA, R. Z. COUTINHO, and A. D. DITCHIFIELD. 2007. Nota sobre dieta e comportamento de forrageio de Artibeus lituratus (Chiroptera, Phyllostomidae) em um parque urbano no sudeste do Brasil. Biota Neotropica, 7: abstract?article+bn01407022007 PRANCE, G. T., and G. B. SCHALLER. 1982. Preliminary study of some vegetation types of the Pantanal, Mato Grosso, Brazil. Brittonia, 34: 228–251. WHITAKER, J. O., and J. S. FINDLEY. 1980. Foods eaten by some bats from Costa Rica and Panama. Journal of Mammalogy, 61: 540–544. Received 21 May 2007, accepted 12 December 2007

partially funded by CNPq-PELD, EWI and FUNDECT; F. Gonçalves, R. Munin and P. Costa were supported by PIBIC-CNPq grants.

AGUIRRE, L. F., A. HERREL, R. VAN DAMME, and E. MATTHYSEN. 2003. The implications of food hardness for diet in bats. Functional Ecology, 17: 201–212. ARAUJO, A. C., and M. SAZIMA. 2003. The assemblage of flowers visited by hummingbirds in the ‘captes’ of Southern Pantanal, Mato Grosso do Sul, Brazil. Flora, 198: 427–435. BORDIGNON, M. O. 2006. Diet of the fishing bat Noctilio leporinus (Linnaeus) (Mammalia, Chiroptera) in a mangrove area of southern Brazil. Revista Brasileira de Zoologia, 23: 256–260. FENTON, M. B., D. AUDET, D. C. DUNNING, J. LONG, C. B. MERRIMAN, D. PEARL, D. M. SYME, B. ADKINS, S. PEDERSEN, and T. WOHLGENANT. 1993. Activity patterns and roost selection by Noctilio albiventris (Chiroptera: Noctilionidae) in Costa Rica. Journal of Mammalogy, 74: 607–613. FISCHER, E. 1992. Foraging of nectarivorous bats on Bauhinia ungulata. Biotropica, 24: 579–582. GRIBEL, R., P. E. GIBBS, and A. L. QUEIROZ. 1999. Flowering phenology and pollination biology of Ceiba pentandra (Bombacaceae) in Central Amazonia. Journal of Tropical Ecology, 15: 247–263. HOOD, C. S., and J. K. JONES. 1984. Noctilio leporinus. Mammalian Species, 216: 1–7. HOOD, C. S., and J. PITOCCHELI. 1983. Noctilio albiventris. Mammalian Species, 197: 1–5.

Seasonal molting in Myotis petax (Chiroptera) in the Russian Far East MIKHAIL P. TIUNOV1, 2 and TATIANA A. MAKARIKOVA1

of Biology and Soil Sciences, Far Eastern Division, Russian Academy of Sciences, Vladivostok 690022, Russia 2 Corresponding author: E-mail:

Key words: Myotis petax, seasonal molting, skin, pregnancy, lactation, Russian Far East

INTRODUCTION Patterns of seasonal molting have been well studied in relatively few species of

Palearctic bats (e.g., Myotis myotis, Pipistrellus nathusii and Nyctalus noctula — Mazak, 1965; Ilyin, 1990). In P. pipistrellus, details of the sequence of events

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