Mammalia: Chiroptera - Canadian Science Publishing

44 downloads 0 Views 271KB Size Report
mean capture rate was higher in savanna and forest sites (0.747 and 0.741 bats/mist-net-hour (mnh), respectively) than in forest fragments (0.483 bats/mnh).
Color profile: Disabled Composite Default screen

1124

Species diversity of bats (Mammalia: Chiroptera) in forest fragments, primary forests, and savannas in central Amazonia, Brazil Enrico Bernard and M. Brock Fenton

Abstract: The exact number of species of bats in Brazilian Amazonia is not precisely known because relatively few sites have been surveyed in detail. Here we present an updated species list of the bats of Alter do Chão at the delta of the Tapajós River in Pará State. Using mist nets and acoustic monitoring of echolocation calls we systematically surveyed 5 forest sites, 14 natural forest fragments, and 12 savanna sites. We captured 3978 bats representing 70 species, 40 genera, and 7 families. Fifty species were recorded in savannas, 44 in forest sites, and 41 in forest fragments. The mean capture rate was higher in savanna and forest sites (0.747 and 0.741 bats/mist-net-hour (mnh), respectively) than in forest fragments (0.483 bats/mnh). Our list includes new records for Brazil and extends knowledge of the distribution of some species. Species-accumulation curves and species-richness estimators indicate that 75–100 bat species occur at Alter do Chão, suggesting that our inventory recorded approximately 67–89% of the bat fauna there. Using cluster analysis we compared the bat fauna at Alter do Chão with the faunas from 17 other sites in the Neotropics. There was 65% similarity with the fauna from Manaus (Brazil), 60% with that from Iwokrama (Guyana), and 57% with that from Paracou (Franch Guiana). Aspects of the conservation status of some species present at Alter do Chão are discussed. Résumé : On ne connaît pas le nombre exact d’espèces de chauves-souris en Amazonie brésilienne, parce que peu de sites ont été inventoriés en détail. Nous présentons ici une liste récente des espèces de chauves-souris d’Alter do Chão, dans le delta de la rivière Tapajós dans l’état de Pará. L’utilisation de filets japonais et l’enregistrement de cris d’écholocation nous ont permis d’inventorier systématiquement 5 sites en forêt, 14 fragments forestiers naturels et 12 sites en savane. Nous avons capturé 3978 chauves-souris représentant 70 espèces, 40 genres et 7 familles. Cinquante espèces ont été trouvées dans les savanes, 44 dans les forêts et 41 dans les fragments. Le nombre moyen de captures était plus élevé dans les savanes et aux sites de forêt (0,747 et 0,741 chauve-souris/filet japonais-heure (mnh), respectivement) que dans les fragments (0,483 chauve-souris/mnh). Notre liste compte de nouvelles mentions pour le Brésil et enrichit nos connaissances sur la répartition d’autres espèces. Les courbes d’accumulation d’espèces et les coefficients de la richesse en espèces indiquent que 75–100 espèces de chauves-souris vivent à Alter do Chão, ce qui permet de croire que notre inventaire a relevé approximativement 67–89 % de la faune de chauves-souris à cet endroit. Nous avons comparé la faune de chauves-souris d’Alter do Chão à celles de 17 autres sites de la zone néotropicale au moyen d’une analyse de groupements. La similarité de la faune d’Alter do Chão avec celle de Manaus (Brésil) est de 65 %, avec celle d’Iwokrama (Guyane), de 60 % et avec celle de Paracou (Guyane française), de 57 %. Quelques aspects de la conservation de certaines des espèces d’Alter do Chão sont examinés. [Traduit par la Rédaction]

Introduction

1140

Emmons 1996; Peres 1997). Rivers also can have an important Bernard and Fenton

The environmental and biogeographic factors determining differences in the diversity and structure of mammal communities in the Amazonian forest are not well known, but soil fertility and its relationship to the availability of food resources have been suggested as important factors influencing species-richness gradients (e.g., Emmons 1984; Voss and Received 11 October 2001. Accepted 14 May 2002. Published on the NRC Research Press Web site at http://cjz.nrc.ca on 4 July 2002. E. Bernard1 and M.B. Fenton. Department of Biology, York University, 4700 Keele Street, Toronto, ON M3J 1P3, Canada. 1

Corresponding author (e-mail: [email protected]).

Can. J. Zool. 80: 1124–1140 (2002)

J:\cjz\cjz8006\Z02-094.vp Friday, June 28, 2002 2:38:39 PM

role in shaping present patterns of species distribution (e.g., Gascon et al. 2000; Patton et al. 2000). However, what is generally known as Amazonian rain forest is actually a composite of different types of vegetation, from evergreen nonflooded tropical forest to partially flooded forest and other types, such as Amazonian savanna (Pires and Prance 1985; Daly and Prance 1989; Tuomisto et al. 1994; Puhakka and Kalliola 1995). Bats are mobile animals with the potential to cover large distances in one night, easily crossing different vegetation types and landscapes that might constitute physical barriers for other species of mammals (e.g., Fleming 1988; Clark et al. 1993; Jong 1994; Fenton 1997; Robinson and Stebbings 1997; Kalko et al. 1999; Law and Lean 1999). As a consequence, bats might not present the same regional patterns of diversity as other mammals of comparable size (e.g., Ditchfield

DOI: 10.1139/Z02-094

© 2002 NRC Canada

Color profile: Disabled Composite Default screen

Bernard and Fenton

2000; Patton et al. 2000; Voss et al. 2001). Further, differences in the morphology and ecology of the species make some of them more suited to using specific habitats such as the spatially complex forest interior or the open areas above the canopy (e.g., Norberg and Rayner 1987; Fenton 1994; Fenton et al. 1998; Bernard 2001c). Brazil harbours ca. 60% of the Amazonian forest, and around 320 species of mammals have been recorded in Brazilian Amazonia (Emmons and Feer 1997), 40% of them bats representing 9 families and 58 genera (Koopman 1993; Marinho-Fillho and Sazima 1998). The exact number of bat species in Brazilian Amazonia is not precisely known because relatively few sites have been surveyed in detail (Handley 1967; Piccinini 1974; Taddei and Reis 1980; Uieda 1980; Mok et al. 1982; Reis 1984; Marques 1986; Reis and Peracchi 1987; Gribel and Taddei 1989). Moreover, some of the published studies used different methodologies, potentially introducing biases into a comparison among sites (Voss and Emmons 1996). As a consequence, the geographic distribution of some species remains poorly documented, making it impossible to predict patterns of bat species richness specific to Brazilian Amazonia from the available data (Simmons and Voss 1998). Bats fill a variety of trophic roles in tropical forests, interacting with a large spectrum of organisms and acting as pollinators, seed dispersers, and predators of insects and small vertebrates (Findley 1993; Altringham 1996). The interactions involving bats and other species in Brazilian Amazonia have only recently been extensively studied (e.g., Reis and Guillaumet 1983; Uieda and Vasconcellos-Neto 1985; Bernard 1997; Gribel et al. 1999; Bernard 2002). Owing to the lack of basic information about the extremely high rates of forest alteration and fragmentation in the area (Whitmore 1997; Laurance et al. 2001), data on the distribution, biology, and ecology of bats in Brazilian Amazonia are urgently needed. These data can help to identify species-rich areas that should be protected and steps that can be taken to protect the remaining biodiversity. As a step towards achieving a better understanding of the distribution of bat species in Brazilian Amazonia and the faunal composition there, we present an updated list of bat species in Alter do Chão at the delta of the Tapajós River in Pará State. Our list includes new records of some species for Brazil and extends our knowledge of the distribution of bats there. We used species-accumulation curves and speciesrichness estimators to evaluate our inventory data and cluster analysis to compare the bat fauna at Alter do Chão with that at other sites in the Neotropics.

Methodology This study was conducted between April and December 2000 near the village of Alter do Chão (2°30′S, 54°57′W) on the right bank of the Tapajós River, 35 m above sea level and 40 km from Santarém, which lies at its confluence with the Amazon River. The average annual temperature varies between 24 and 27°C and the average annual rainfall is about 2000 mm (Miranda 1993). During the dry season (July to November) the area receives only 25% of the annual rainfall. Different types of vegetation are present, but the predomi-

1125

nant formations are tropical forest and Amazonian savannas (Pires and Prance 1985). The savanna vegetation is composed mainly of grasses (Paspalum carinatum and Trachypogon plumosus) with sparse clumps of shrubs belonging principally to the families Myrtaceae and Rubiaceae (Miranda 1993; Magnusson et al. 1999). Patches of forest ranging from 0.5 to 360 ha in area occur within the savannas. Trees of at least 57 families occur in the forest fragments, the 3 most common being Myrtaceae, Flacoutiaceae, and Leguminosae (W.E. Magnusson and J. Camara, unpublished data). Amazonian savannas have limited distributions and the area around Alter do Chão has been suggested for designation as a faunal sanctuary (Rylands and Pinto 1998). This area was previously sampled in 1998 (Bernard 2001a; Bernard et al. 2001). We systematically surveyed 5 forest sites, 14 natural forest fragments (6–360 ha), and 12 savanna sites covering ca. 30000 ha (Fig. 1). Locations of the sites were determined with a global positioning system (GPS) receiver (model GPS 12, Garmin, Olanthe, Kansas, U.S.A.), and sites were plotted on a map of the area (Albernaz 2002), with the different vegetation types and boundaries based on a LANDSAT image geo-processed using IDRISI (Eastmann 1995) and ArcView 3.2 (Environmental Systems Research Institute, Inc. 1996). Distances between sites varied from 0.25 to 14 km. With a few exceptions, each site was visited 5 times, with 30-day intervals between successive visits. No sampling was performed between the third quarter and full moon of each lunar cycle. All bats were captured with mist nets set along existing 150 m long transect trails located at the centre of each of the forest sites and forest fragments and in the surrounding savannas. We used 12 × 2.5 m mist nets set at ground level, which were opened at 18:00 and closed at 24:00. Nets were closed during rain or wind storms. After being alerted by local residents to the presence of colonies of molossids in the vicinity, we complemented our sampling with 2 nights of sampling (1 h each night) in a backyard in the village. We included this site because molossids usually fly high above the reach of mist nets and because we were interested in describing the species diversity of this locally poorly sampled family. We also monitored the echolocation calls of aerial-feeding insectivorous species to complement our inventory. We used two different systems. One was an Anabat II bat detector with Anabat Zero Crossing Analysis Interface Module and Anabat 6 DOS software installed on a portable computer. The other used the high-frequency output of a QMC S200 bat detector recorded on a Racal Store 4D tape recorder running at 30 in./s (1 in. = 25.4 mm). Recorded calls were analysed with Canary version 2.1 software. Both detection systems were used in savannas, forest, and forest fragments as well as in flooded forest and along the banks of the Tapajós River and the margins of adjoining lakes. The echolocation calls recorded were identified by comparison with those reported in the literature (e.g., Kalko 1995; O’Farrell and Miller 1997; Kalko et al. 1998; O’Farrell and Miller 1999; Ochoa et al. 2000). Nets were checked at 20- to 30-min intervals and all captured bats were placed in individual cloth bags for later identification and measurement. Bats were subsequently released at the capture site no more than 2 h later. Small species and © 2002 NRC Canada

J:\cjz\cjz8006\Z02-094.vp Friday, June 28, 2002 2:38:40 PM

Color profile: Disabled Composite Default screen

1126

Can. J. Zool. Vol. 80, 2002

Fig. 1. Study area on the right bank of the Tapajós River in Pará State, Brazil. Darker shaded areas represent primary forests and forest fragments and lighter shaded areas represent savannas. Dots mark the sites sampled (see the text).

nectarivores were processed quickly to minimize mortality. Identification of all species was based on an unpublished key to Amazonian bats (C. Handley, personal communication). The nomenclature used herein follows Koopman (1993) and Simmons and Voss (1998). Body mass (g), sex, age, and forearm length (mm) were recorded for each individual. With the exception of subadults (with non-ossified carpal epiphyses) and very small species, captured individuals were marked with a ball-chain necklace with a predetermined number (Handley et al. 1991). Voucher specimens of rare species, together with those whose identification was problematic and others that died during handling, were preserved in 70% ethanol and deposited in the Coleção de Mamíferos of the Instituto Nacional de Pesquisas da Amazônia (INPA) in Manaus. Species-accumulation curves were obtained by plotting the cumulative number of captured species against the total number of captures. We smoothed the curves by randomizing them 100 times (see Colwell and Coddington 1996). Because mist nets are selective and tend to undersample aerialfeeding insectivores (Kunz and Kurta 1988; Kalko 1995; Voss and Emmons 1996; Simmons and Voss 1998), we present accumulation curves based on two sets of data: all captures (except those from backyard nets) and captures of phyllostomids (the dominant family) only. We also plotted accumulation curves for total captures and captures in each habitat (savanna, forest, and forest fragments) separately. The form and structure of the curves provide a good indication of the quality of the inventory and how well local communities were sampled (Longino and Colwell 1997; Moreno and Halffter 2000; Sampaio 2000). Species-accumulation curves, together with parametric and non-parametric models, can also be used

to assess the number of species expected in an area (Bunge and Fitzpatrick 1993; Chao et al. 1993; Colwell and Coddington 1996; Simmons and Voss 1998; Lim and Engstrom 2001b). We used the following species estimators: abundance coverage; incidence coverage; Chao 1 and Chao 2; jackknife 1; and bootstrap (e.g., Chao 1984, 1987; Bunge and Fitzpatrick 1993; Chao et al. 1993). Colwell and Codington (1996) provide a detailed description of the estimators used here. Speciesrichness estimators were calculated with the program EstimateS (Colwell 1997), using all the species except those from backyard nets, and species-accumulation curves were plotted using the program BiodiversityPro (McAleece 1997). To assess patterns of biogeographic similarity between the bat fauna of Alter do Chão and faunas at other Neotropical sites, we followed the analysis of Lim and Engstrom (2001b), which complemented that of Simmons and Voss (1998), expanding their original matrix with regional information from biosphere reserves, national parks, concession blocks, and forest reserves. The similarity of Lim and Engstrom’s (2001b) and Simmons and Voss’ (1998) results suggest that the data used provide robust representations of biogeographic trends. However, we excluded Maracá and Xingú from our analysis because, as pointed by Lim and Engstrom (2001b), their species lists are probably too incomplete to reliably indicate fine patterns of faunal similarity at the species level. We complemented Lim and Engstrom’s (2001b) matrix with our data and updated the Manaus list, based on the results of a more complete inventory for that area (Sampaio et al. 2002). Data from French Guiana were also updated with data from Saül and corrections for Arataye (Simmons et al. 2000). We used Jaccard’s coefficient (Jij = Cij /Tij, where Cij is the number of species common to both faunas and Tij is the total © 2002 NRC Canada

J:\cjz\cjz8006\Z02-094.vp Friday, June 28, 2002 2:38:59 PM

Color profile: Disabled Composite Default screen

Bernard and Fenton

1127

Table 1. Summary of the results of mist-net sampling at Alter do Chão, Pará State, Brazil. Habitat Forest Forest fragments Savanna Backyard

No. of sites 5 14 12 1

Effort (mist-net-hours)a

No. of captures

No. of species

No. of unique speciesb

1523 2444.5 2146.5 2

1129 1183 1605 61

44 41 50 5

8 7 9 3

Capture ratioc 0.741 0.483 0.747 30.5

Species ratio 1d

Species ratio 2e

0.028 0.016 0.023 2.5

0.038 0.034 0.031 0.081

a

One 12 × 2.5 m net open for 1 h equals 1 mist-net-hour (mnh)). Species recorded exclusively in a given habitat. c Number of captures divided by effort. d Number of species divided by effort. e Number of species divided by number of captures. b

number of species in the two faunas combined (Tij = Ni + Nj – Cij)) to calculate faunal similarity between each pair of sites. A species by site matrix was created from 18 sites (Appendix A) and sites were clustered by the unweighted pair group method with arithmetic average (UPGMA), using Statistica 5.1 software (StatSoft Inc. 1998).

Fig. 2. Histograms representing the relative contributions of four different phyllostomid subfamilies to the total numbers of bats (Glossophaginae (gloss); Carolliinae (car); Phyllostominae (phy); and Stenodermatinae (ste)) captured in three habitats (savannas, forests, and forest fragments) at Alter do Chão, Pará State, Brazil, based on total captures (A) and captures in each habitat (B).

Results Our capture effort at Alter do Chão in 2000 was 6116 mist-net-hours (mnh) over 102 nights of sampling (Table 1). We captured 3978 bats (including 153 recaptures) representing 70 species, 40 genera, and 7 families (Table 2). The four most frequently captured species were Carollia perspicillata, Artibeus lituratus, Carollia brevicauda, and Artibeus jamaicensis, representing 58.2% of total captures. Carollia perspicillata alone accounted for 22.9% of total captures. The 10 most frequently captured species accounted for 81.7% of captures, while 41 other species had fewer than 10 captures each and accounted for 2.9% of captures (Table 2). The most speciose family was Phyllostomidae (49 species), followed by Emballonuridae and Vespertilionidae (6 species each), Molossidae (4 species each), Mormoopidae and Thyropteridae (2 species each), and Noctilionidae (1 species). Among the Phyllostomidae, the subfamily Phyllostominae was represented by the most species (22), followed by Stenodermatinae (17), Glossophaginae (5), Carolliinae (4), and Desmodontinae (1). However, based on numbers of captures, Stenodermatinae was the most abundant subfamily (1618 captures), followed by Carolliinae (1469), Phyllostominae (607), Glossophaginae (119), and Desmodontinae (19). The mean capture rate was higher in savanna and forest sites (0.747 and 0.741 bats/mnh, respectively) than in forest fragments (0.483 bats/mnh). The capture rate in the backyard was extremely high (30.5 bats/mnh) compared with other sites because we set mist nets close to a known roost. The total number of species recorded in each habitat varied between 50 in savannas and 41 in forest fragments, resulting in 0.023 species/mnh in savannas, 0.028 species/mnh for forest sites, and 0.016 species/mnh in forest fragments. We obtained 0.038 species/capture in forests, 0.034 species/capture in forest fragments, and 0.031 species/capture in savannas (Table 1). The taxonomic composition of the bat species assemblages varied among the three habitats, based on both total captures and captures in each habitat separately. In savanna sites, stenodermatines accounted for 50.9% of captures, carolliines

for 26.5%, and phyllostomines for 16.8%. In forest sites, carolliines represented 51.9% of captures, stenodermatines 28.3%, and phyllostomines 11.5%. Forest fragments showed a less pronounced difference between stenodermatines and carolliines (40.6 and 38.5%, respectively), with phyllostomines representing 17.4% of the captures in that habitat (Fig. 2). Nine species were captured exclusively in savanna sites, eight only in forest sites, five only in forest fragments, and three were captured only in the backyard. Factors explaining the differences observed among habitats are complex and a complete analysis of this topic, as well as the possible effects of forest fragmentation on the studied area, will be presented elsewhere. Echolocation calls indicated that the aerial-feeding insectivores Saccopteryx bilineata, Saccopteryx canescens, and an unidentified Peropteryx species are more abundant than was indicated by mist-net captures, these species being frequent at forest-fragment edges and in savannas. We positively identified calls of nine species of bats, including the mormoopid © 2002 NRC Canada

J:\cjz\cjz8006\Z02-094.vp Friday, June 28, 2002 2:39:23 PM

Color profile: Disabled Composite Default screen

1128

Can. J. Zool. Vol. 80, 2002

Table 2. Numbers of bat captures in primary forests, forest fragments, and savannas at Alter do Chão, central Amazonia, Brazil, between April and December 2000.

Carollia perspicillata (Linnaeus, 1758) Artibeus lituratus (Olfers, 1818) Carollia brevicauda (Schinz, 1821) Artibeus jamaicensis Leach, 1821 Phyllostomus discolor Wagner, 1843 Artibeus cinereus (Gervais, 1856) Artibeus obscurus (Schinz, 1821) Artibeus concolor Peters, 1865 Glossophaga soricina (Pallas, 1766) Rhinophylla fischerae Carter, 1966 Tonatia silvicola (d’Orbigny, 1836) Phyllostomus elongatus (E. Geoffroy, 1810) Uroderma magnirostrum Davis, 1968 Ametrida centurio Gray, 1847 Mimon crenulatum (E. Geoffroy, 1810) Uroderma bilobatum Peters, 1866 Noctilio albiventris Desmarest, 1818 Pteronotus parnellii (Gray, 1843) Artibeus anderseni Osgood, 1916 Tonatia saurophila Koopman & Williams, 1951 Trinycteris nicefori (Sanborn, 1949) Molossus molossus (Pallas, 1766) Desmodus rotundus (E. Geoffroy, 1810) Sturnira lilium (E. Geoffroy, 1810) Platyrrhinus helleri (Petters, 1866) Vampyressa bidens (Dobson, 1878) Choeroniscus minor (Peters, 1868) Rhynchonycteris naso (Wied, 1820) Lichonycteris obscura Thomas, 1895 Rhinophylla pumilio Peters, 1865 Peropteryx sp. Artibeus gnomus Handley, 1987 Chiroderma villosum Peters, 1860 Saccopteryx bilineata (Temminck, 1838) Tonatia brasiliense (Peters, 1867) Ectophylla macconnelli (Thomas, 1901) Platyrrhinus brachycephalus Rouk & Carter, 1972 Scleronycteris ega Thomas, 1912 Eptesicus brasiliensis (Desmarest, 1819) Lonchophylla thomasi J.A. Allen, 1904 Micronycteris minuta (Gervais, 1856) Phyllostomus hastatus (Pallas, 1767) Phylloderma stenops Peters, 1865 Saccopteryx canescens Thomas, 1901 Trachops cirrhosus (Spix, 1823) Vampyrum spectrum (Linnaeus, 1758) Cynomops planirostris (Peters, 1866) Lampronycteris brachyotis (Dobson, 1879) Micronycteris schmidtorum Sanborn, 1935 Glyphonycteris sylvestris Thomas, 1896 Peropteryx macrotis (Wagner, 1843) Eumops bonariensis (Peters, 1874) Myotis n.sp. Chrotopterus auritus (Peters, 1856) Chiroderma trinitatum Goodwin, 1958

Family/subfamilya

Savanna

Forest fragment

Forest

PHY/Car PHY/Ste PHY/Car PHY/Ste PHY/Phy PHY/Ste PHY/Ste PHY/Ste PHY/Glo PHY/Car PHY/Phy PHY/Phy PHY/Ste PHY/Ste PHY/Phy PHY/Phy NOC MOR PHY/Ste PHY/Phy PHY/Phy MOL PHY/Des PHY/Ste PHY/Ste PHY/Ste PHY/Glo EMB PHY/Glo PHY/Car EMB PHY/Ste PHY/Ste EMB PHY/Phy PHY/Ste PHY/Ste PHY/Glo VES PHY/Glo PHY/Phy PHY/Phy PHY/Phy EMB PHY/Phy PHY/Phy MOL PHY/Phy PHY/Phy PHY/Phy EMB MOL VES PHY/Phy PHY/Ste

276 279 136 169 199 91 48 102 47 13 4 4 37 45 4 24 1 9 10 11 13 0 2 12 4 8 2 12 1 1 0 3 4 6 4 1 3 1 3 1 0 1 0 1 0 3 1 1 0 0 0 2 0 0 1

282 186 128 107 66 71 64 17 11 43 62 30 8 1 20 7 0 0 15 9 2 0 0 0 5 3 5 2 4 3 8 2 1 0 1 0 1 3 0 0 1 2 2 2 3 0 0 0 0 0 2 0 0 1 0

356 169 202 28 29 27 32 17 35 24 13 33 14 0 19 5 0 21 3 8 11 0 17 6 8 4 7 0 6 5 0 2 2 1 2 5 2 0 0 2 2 0 1 0 0 0 0 1 2 2 0 0 0 0 0

Backyard 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 31 0 0 0 0 25 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 2 0 0 0 0 0 2 0 0

Total 914 634 466 304 294 189 144 136 93 80 79 67 59 46 43 36 32 30 28 28 26 25 19 18 17 15 14 14 11 9 8 7 7 7 7 6 6 4 3 3 3 3 3 3 3 3 3 2 2 2 2 2 2 1 1

© 2002 NRC Canada

J:\cjz\cjz8006\Z02-094.vp Friday, June 28, 2002 2:39:24 PM

Color profile: Disabled Composite Default screen

Bernard and Fenton

1129

Table 2 (concluded).

Cynomops paranus (Thomas, 1901) Diclidurus ingens Hernandez-Camacho, 1955 Eptesicus cf. chiriquinus Thomas, 1920 Glyphonycteris daviesi (Hill, 1964) Lasiurus cf. blossevilli Myotis albescens (E. Geoffroy, 1806) Micronycteris hirsuta (Peters, 1869) Micronycteris homezi Pirlot, 1967 Micronycteris megalotis (Gray, 1842) Myotis riparius Handley, 1960 Pteronotus gymnonotus Natterer, 1843 Sturnira tildae de la Torre, 1959 Tonatia carrikeri (J.A. Allen, 1910) Thyroptera lavali Pine, 1992 Thyroptera tricolor Spix, 1823 Total

Family/subfamilya MOL EMB VES PHY/Phy VES VES PHY/Phy PHY/Phy PHY/Phy VES MOR PHY/Ste PHY/Phy THY THY 7

Savanna 0 0 1 0 1 0 0 1 0 0 1 0 1 0 0 1605

Forest fragment 0 1 0 0 0 0 0 0 1 0 0 0 0 0 1 1183

Forest 0 0 0 1 0 1 1 0 0 1 0 1 0 1 0 1129

Backyard 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 61

Total 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 3978

a Families are as follows: EMB, Emballonuridae; MOL, Molossidae; MOR, Mormoopidae; NOC, Noctilionidae; THY, Thyropteridae; VES, Vespertilionidae; and PHY, Phyllostomidae. Subfamilies are as follows: Car, Carollinae; Des, Desmodontinae; Glo, Glossophaginae; Phy, Phyllostomidae; Ste, Stenodermatinae.

Pteronotus davyi, which was recorded flying on 3 nights but was never captured in nets. The echolocation-call data also indicated that the molossid fauna in Alter do Chão is composed of at least 10 species; however, we were not able to identify most of the calls to species because individuals were never captured and some molossids have a wide variation in their call repertoire. Species-saturation curves based on captures of phyllostomids reached values close to the asymptote for the three habitats, suggesting that this family was almost completely sampled and few more species would have been added by extending the sampling effort (Fig. 3). Curves based on total captures presented steeper slopes than curves based on phyllostomids. Species-richness estimators used with our data predict 75– 100 bat species at Alter do Chão (Table 3), suggesting that our inventory recorded approximately 67–89% of the bat fauna there. Cluster analysis produced three major groups of study sites, based mainly on geographic proximity (Fig. 4): Central America (Barro Colorado Island in Panamá, La Selva in Costa Rica, and Montes Azules in México), western Amazonia (Balta, Cuzco Amazonico, Jenaro Herrera, Manú, all Peruvian sites, and Yasuni in Ecuador), and eastern Amazonia (Alter do Chão and Manaus in Brazil, Arataye, Piste Saint Élie, Säul, and Paracou in French Guiana, Cunucunama, Imataca, and San Juan de Manapiare in Venzuela, and Iwokrama in Guyana). The bat fauna of Alter do Chão shows 65% similarity with the fauna from Manaus, 60% with that from Iwokrama, and 57% with that from Paracou (Table 4).

Discussion Based on captures with mist nets, Alter do Chão has at least 72 species of bats from 41 genera and 7 families (Bernard 2001a; this study), but species-accumulation curves and species-richness estimators indicate that the bat fauna there

has not yet been totally inventoried. Based on species recorded at sites close to Alter do Chão and on our echolocation data, we expect 10–15 species to be added to the present list. As in other surveys of bats, a few common and abundant species dominate our sample (e.g., Aldridge and Rautenbach 1987; Rautenbach et al. 1996; Moreno and Halffter 2000). A comparison of our data from Alter do Chão with captures in ground-level mist nets at four other Neotropical sites (Manaus, Paracou, Iwokrama, and Barro Colorado Island) shows that the five most abundant species recorded belong to just three or four genera, mostly phyllostomids (Table 5). At each site, the top five species accounted for 52–82% of total captures. The rank order and species vary from site to site, but the 5 commonest species belong to a short list (13 species) of which the single most abundant species is always C. perspicillata, A. jamaicensis, or A. lituratus. These superabundant species have broad geographic distributions and are always among the most frequent taxa at other Amazonian sites (e.g., Handley 1967; Reis 1984; Reis and Peracchi 1987; Brosset and CharlesDominique 1990; Ascorra et al. 1993, 1996; Cosson et al. 1999). The proportion of singleton species in our Alter do Chão sample (24%) was higher than at any of the other four sites mentioned above, where singletons accounted for 7–20% of species (Table 5). Comparing species lists among sites, we observe that singleton species at one site (e.g., Ectophylla macconnelli and Chrotopterus auritus) may be more abundant at others, suggesting that this is probably not an accurate criterion for classifying a species as rare. Further, capture methods have a direct influence on the numbers of bats recorded. At Paracou, when captures with mist nets are considered, both Peropteryx leucoptera and E. macconnelli were singletons. However, roost searching produced larger groups of the same species (Simmons and Voss 1998). In lowland forests in northeastern Costa Rica, roost searching for the disk-winged © 2002 NRC Canada

J:\cjz\cjz8006\Z02-094.vp Friday, June 28, 2002 2:39:25 PM

Color profile: Disabled Composite Default screen

1130

Can. J. Zool. Vol. 80, 2002

Fig. 3. Species-accumulation curves based on numbers of bats captured in three habitats (savannas, forests, and forest fragments; “total” represents all habitats pooled) at Alter do Chão, Pará State, Brazil, based on all species (A) and phyllostomids only (B).

bat Thyroptera tricolor showed densities up to 33 bats/ha (Vonhof 2001), much higher than those observed by mistnetting at other sites in the Neotropics. Therefore, a species should not be classified as rare on the basis of a single capture technique. We reached 90% of observed species (i.e., 63 species) after ca. 2700 captures and 70 nights of effort. Compared with Paracou (Simmons and Voss 1998) and Manaus (Sampaio et al. 2002), more effort is apparently needed at Alter do Chão, in terms of both number of captures and mist-net-hours, to reach 90% species completeness. However, compared with Barro Colorado Island (Kalko et al. 1996), less effort was needed to reach the same completeness level. In Paracou, Simmons and Voss (1998) recorded 3126 captures and 78 species over168 sampling days. About 78% of their captures were in ground-level mist nets, 10% in elevated nets, and

12% at roosts. Based on ground-level nets, 90% of the observed fauna (58 species) was reached after 1054 captures and 57 nights (Simmons and Voss 1998, p. 172) and the total number of observed species at ground level (65) after 2444 captures. At Manaus, where the ground-level capture effort in two reserves included 250 nights of sampling and ca. 26 500 mnh, 90% of the observed species were reached after ca. 2000 captures (Sampaio et al. 2002). After that, species were added slowly, about 6000 captures being required to reach 95% completeness. In a 10-year study involving over 48 000 captures on Barro Colorado Island, Panamá, it took 2 nights, on average, to catch 10 species, 7 nights to reach 20 species, and 22 nights to record 30 species (Kalko et al. 1996: 516). We reached 30 species after just 8 nights of captures and 48 species after 30 nights. Other authors recording bat inventories using mist nets in © 2002 NRC Canada

J:\cjz\cjz8006\Z02-094.vp Friday, June 28, 2002 2:39:58 PM

Color profile: Disabled Composite Default screen

Bernard and Fenton

1131

Fig. 4. Phenogram derived from unweighted pair group with UPGMA cluster analysis for 18 Neotropical bat faunas (see the text for references). The bottom scale shows the clustering level as percent faunal similarity based on Jaccard’s index × 100. The matrix used to generate this cluster is presented in Appendix A.

Table 3. Expected numbers of of bats at Alter do Chão, Pará State, Brazil, based on different species-richness estimators. Estimator Abundance coverage Incidence coverage Chao 1 Chao 2 Jackknife 1 Bootstrap

All habitats (67 species) 88 (76) 93 (72) 94 (71) 100 (67) 87 (77) 75 (89)

Forest sites (44 species)

Savannas (50 species)

Forest fragments (41 species)

51 54 49 54 55 49

71 69 93 82 66 57

49 49 47 45 50 46

(86) (81) (90) (81) (80) (90)

(70) (72) (53) (61) (76) (88)

(84) (84) (87) (91) (82) (89)

Note: Numbers in parentheses represent the percentage of completeness for each habitat, based on the number of species recorded. Decimal fractions were rounded.

the Neotropics complemented their captures with the use of different sampling techniques, such as harp traps, shooting, roost searching, and acoustic monitoring (e.g., Kalko et al. 1996; Simmons and Voss 1998; Lim and Engstrom 2001a, 2001b). At Paracou, 5 of the 78 species found were captured exclusively at roosts (Simmons and Voss 1998). In Panamá, some species were never captured with mist nets but are considered common, based on echolocation recording (Kalko et al. 1996). Studies on the vertical stratification of bats also show that the spatial distribution of several species is not uniform and that the probability of capturing some species is higher with the use of canopy nets (Handley 1967; Bernard 2001c; Lim and Engstrom 2001b). Noteworthy records We added 30 species of bats to the previous list for Alter do Chão sites (Bernard 2001a), and only Cormura brevirostris and P. leucoptera were captured in 1998 but not in the present study. The present list includes species whose distribution is poorly known (e.g., Pteronotus gymnonotus, Diclidurus ingens,

and Eumops bonariensis) and others known from only a few other sites. For example, we report the first specimen of Thyroptera lavali (Thyropteridae) for Brazil. This species was previously represented by a few specimens from one locality in northern Perú (Pine 1993) and three specimens from Yasuni National Park, Napo Province, Ecuador (Reid et al. 2000). Alter do Chão is ca. 2100 km northeast of Loreto Department in Perú, the type locality, and to date T. lavali is known from just three localities. We also recorded a second specimen of Micronycteris homezi from Alter do Chão. This species was captured for the first time in Brazil during our previous survey at this site (Bernard 2001b), extending its range by ca. 2000 km southsoutheast of its type locality in Venezuela and ca. 800 km from subsequent captures in French Guiana and Guyana (Simmons and Voss 1998; Lim and Engstrom 2001a). We also collected eight specimens of an apparently undescribed species of Peropteryx that is similar to the species described as Peropteryx cf. macrotis in Reid et al. (2000). Those authors indicated that their specimen exhibited white wings © 2002 NRC Canada

J:\cjz\cjz8006\Z02-094.vp Friday, June 28, 2002 2:40:02 PM

Color profile: Disabled Composite Default screen

Note: Values are given as Jaccard’s similarity coefficient × 100. Locations are as follows: Brazil: Alter, Alter do Chão; Mana, Manaus; Costa Rica: LaSe, La Selva; Ecuador: Yasu, Yasuni; French Guiana: Arat, Arataye; Para, Paracou; Saul; StEl, Piste Saint Élie; Guyana: Iwok, Iwokrama; Mexico: Mazu, Montes Azules; Panamá: BCI, Barro Colorado Island; Perú: Balt, Balta; Cuzc, Cuzco Amazônico; JHer, Jenaro Herrera; Manú; Venezuela: Cunu, Cunucunuma; Imat, Imataca; SJMa, San Juan de Manapiare.

Alter

28.3 35.6 36.3 54.6 51.8 57.2 49.4 41.8 65.2 50.5 48.2 45.1 46.2 59.7 52.1 54.9 44.8

Saul Yasu

27.8 38.1 37.5 58.0 53.7 54.1 49.4 46.9 52.4 55.9 53.6 57.4 52.0 52.0 41.4 33.6 36.0 41.0 56.8 45.3 50.0 50.0 45.7 54.4 43.0 45.4 45.6 36.4 58.7

SJMa Iwok

33.6 37.0 40.3 67.7 53.9 63.6 53.1 47.7 68.0 46.4 47.3 45.9 40.6 26.7 32.5 35.0 43.0 47.7 37.7 39.4 39.7 44.4 55.0 61.9 53.0

Cuzc Manú

33.6 41.1 42.0 53.9 46.1 42.3 41.4 46.5 50.4 53.2 58.1 30.1 32.6 36.3 53.4 48.0 43.1 43.9 42.6 51.0 58.6

Balt JHer

26.0 33.6 37.3 48.9 52.6 50.0 46.4 41.7 54.7 31.8 42.8 42.3 59.8 56.1 67.3 53.6 46.7

Mana Cunu

28.0 32.1 36.1 52.3 52.9 43.3 54.1 26.2 31.2 34.7 61.6 61.9 59.0

Arat Para

31.1 41.1 37.8 60.2 62.1 25.5 40.0 36.0 59.0

StEl Imat

31.4 43.0 42.4 39.5 64.1

BCI LaSe

43.3 Mazu LaSe BCI Imat StEl Para Arat Cunu Mana Jher Balt Manú Cuzc Iwok SJMa Yasu Saul

Table 4. Percentages of faunal similarity among 18 Neotropical rainforest bat faunas.

Can. J. Zool. Vol. 80, 2002

25.5 32.2 34.4 50.0 56.5 54.6 61.9 44.4 47.8 43.2 40.5 41.4 39.4 48.9 43.6 48.1

1132

with pigments only along the forearms and digits and the ears not joined over the crown, while in P. leucoptera the digits are nonpigmented and the ears are joined. We also collected two specimens of a small, apparently undescribed Myotis species (forearm 33 mm long) that generally resembles Myotis albescens but differs in wing colour. Missing species Although our sampling appears to have produced 67–89% of the species expected, we do not know precisely which additional species to expect at Alter do Chão; however, we can use distribution data from elsewhere in Amazonia (Mok et al. 1982; Koopman 1993; Marinho-Filho and Sazima 1998; Simmons and Voss 1998; Bernard 2001a; Bernard et al. 2001; Sampaio et al. 2002) to make some predictions. Because our mist-netting was restricted to ground level, we expect that the most of the species missing from our sampling are aerial-feeding insectivores, including verpertilionids, emballonurids, and molossids. The Amazon National Park, ca. 200 km southwest of Alter do Chão on the left bank of the Tapajós River, is the closest site to Alter do Chão that was surveyed for bats (Reis and Schubart 1979; Marques 1986; Bernard 2001a). From those data, we expect that Saccopteryx leptura, Pteronotus personatus, Macrophyllum macrophyllum, Lonchorhina aurita, Myotis nigricans, Nyctinomops laticaudatus, and Molossus ater will eventually be recorded at Alter do Chão. Neoplatymops mattogrossensis has been taken on the east bank of the Xingú River, ca. 350 km east of Alter do Chão (Voss and Emmons 1996), and Promops centralis occurs across Amazonia from east to west (Gregorin 1998; Gregorin and Taddei 2000), so both species may occur at Alter do Chão. At Paracou, Simmons and Voss (1998) recorded nine species of molossids but expected eight other species, based on adjacent records. Three of the four species of molossids we recorded were captured in the backyard nets when the bats were leaving roosts. We observed signs of several other colonies in the roofs of houses in the village, and future studies of the local diversity of this family should definitively include searching and capturing inside the village. Saccopteryx gymnura is a rare species, known from just a few specimens and originally described from Santarém (Thomas 1901). Diclidurus albus is widespread across the Amazon Basin, and residents from Alter do Chão reported that a “white bat” (possibly D. albus) is frequently observed hanging in palm fronds in forest sites and forest fragments. Other poorly known congeners such as Diclidurus isabelus and Diclidurus scutatus, together with the rare yet widespread Centronycteris maximiliani (see Simmons and Handley 1998), are among the other emballonurids that may occur at Alter do Chão. Lasiurus ega has a widespread distribution in South America (Kurta and Lehr 1995) and may complement the list of vespertilionids at Alter do Chão. We also expect Noctilio leporinus, which we may have missed because we did not net over water. Very small but geographically widespread species such as Natalus stramineus and Furipterus horrens are frequently absent from species lists because they are rarely captured with mist nets. Simmons and Voss (1998) recorded the latter species based on captures in roosts or in or under fallen trees in various stages of decomposition, and © 2002 NRC Canada

J:\cjz\cjz8006\Z02-094.vp Friday, June 28, 2002 2:40:03 PM

Color profile: Disabled Composite Default screen

Bernard and Fenton

1133

Table 5. Numbers of ground-level captures of bats at five Neotropical sites, including the five most abundant species, the percentages of total captures that they represent, and the proportions of species recorded only once (singletons). Alter do Chão No. of captures Effort (mnh) Ranking 1 2 3 4 5 Percentage of captures Percentage of singletons Source

3978 6116

Manaus 7 039 26 500

C. perspicillata A. lituratus C. brevicauda A. jamaicensis P. discolor 65 24 This study

C. perspicillata R. pumilio A. obscurus C. brevicauda P. parnellii 74 na Sampaio et al. 2002

Paracou

Iwokrama

Barro Colorado

2444 2080

1336 8500

9118 na

C. perspicillata P. elongatus R. pumilio A. obscurus M. molossus 61 15 Simmons and Voss 1998

A. lituratus C. perspicillata A. obscurus A. planirostris P. parnellii 52 20 Lim and Engstrom, 2001b

A. jamaicensis A. lituratus U. bilobatum C. perspicillata V. caraccioli 82 7 Handley et al. 1991

Note: See the references for site descriptions.

F. horrens was recorded in the Xingú and Manaus inventories (Voss and Emmons 1996; E.M. Sampaio, personal communication). Although our saturation curves suggest that the phyllostomid fauna is the best inventoried in this study, Anoura caudifera, Vampyressa brocki, and Diphylla ecaudata are widespread species known from Xingú and Manaus that should also occur at Alter do Chão. Cluster analysis Cluster analysis suggests that Neotropical bat faunas fall into three main groups reflecting biogeographic affinities (Central America, eastern Amazonia, and western Amazonia), a result that resembles those of Simmons and Voss (1998) and Lim and Engstrom (2001b). Our analysis, however, presents a slightly different pairing of sites. Specifically, sites from eastern Amazonia clustered in two main groups (Fig. 4): Imataca, Iwokrama Forest, Paracou, Manaus, and Alter do Chão form the first group; Piste St. Élie and Arataye, Säul, Cunucunuma, and San Juan de Manapiare represent the second. The grouping of sites from French Guiana with Cunucunuma and San Juan de Manapiare in Venezuela probably reflects an artefact of inventory completeness (Simmons et al. 2000; Lim and Engstrom 2001b), and cluster analysis may be sensitive to incomplete data. Missing from our analysis are points from the extreme east of the Amazon Basin, close to the delta of the Amazon River, and future studies in that area are very necessary to address possible differences between the faunas from eastern, central and western Amazonia (Bernard et al. 2001). Conservation status of the bat fauna from Alter do Chão The Brazilian official list of species vulnerable to extinction includes nine species of bats: S. gymnura, Vampyrum spectrum, Lonchophylla bokermanni, Chiroderma doriae, Plathyrrhinus recifinus, Lasiurus ebenus, Lasiurus egregius, Myotis ruber, and Lichonycteris obscura (Aguiar et al. 1998). Eighteen other species are considered probably vulnerable, but most of them were listed because of insufficient data about their biology, ecology, and distribution and, consequently, their conservation status. Two of the species considered vulnerable (V. spectrum and L. obscura) and three of the species considered probably vulnerable (D. ingens, Lampronycteris

brachyotis, Scleronycteris ega) were recorded in our study at Alter do Chão. Vampyrum spectrum was included in the Brazilian official list based on small population size, high dependence on protected habitats, and occurrence in habitats suffering moderate disturbance (Aguiar et al. 1998). The criteria used to include L. obscura were rarity, total dependence on protected areas, and occurrence in habitats suffering moderate disturbance. However, an analysis of the data available for these species indicates that a careful reexamination of their status is necessary. No data on population sizes are available for V. spectrum and L. obscura anywhere in Brazil, and the fact that they are represented by few specimens in collections may be a consequence of sampling bias. Moreover, despite the few records, V. spectrum is widespread in Amazonia and also occurs in the Pantanal biome, while L. obscura has been recorded in Amazonia and the Atlantic Forest. It is true that all those biomes have experienced strong human pressure in the last decades (e.g., Laurance et al. 2001), but again no studies are available on the effect of such pressure on those species. Because V. spectrum is a carnivore, it is expected to require large feeding areas and present naturally low densities, being more vulnerable to local habitat change. However, the present status of knowledge about the biology and ecology of this species in Brazil, as well as for L. obscura, does not provide reliable support when the criteria specified as necessary to classify them as vulnerable species are taken into account (Hutson et al. 2001). We still know much less about Neotropical species than is necessary for developing effective conservation plans.

Acknowledgements We thank Edvaldo Farias and Adnor Costa for their valuable help during all the fieldwork in Alter do Chão. Dr. W.E. Magnusson provided logistical support through the Biodiversity of Amazonian Savannas project (INPA PPI 2-3540, Conselho Nacional de Desenvolvimento Científico e Tecnológico grant 521102-95.2) from the Instituto Nacional de Pesquisas da Amazônia (INPA) in Manaus, Brazil. Drs. R. Voss, N. Simmons, and W.E. Magnusson gently reviewed the earlier version of the manuscript, while Drs. C.E. Moreno and R.K. Colwell provided comments on its final version. Work in Alter do © 2002 NRC Canada

J:\cjz\cjz8006\Z02-094.vp Friday, June 28, 2002 2:40:03 PM

Color profile: Disabled Composite Default screen

1134

Chão was possible thanks to grants from the Department of Biology, York University, and a Ph.D. grant from Coordenação de Aperfeiçoamento de Pessoal de Nível Superior Foundation (Brazil) to E.B. Collections were made under permit 143/2000 DIFAS/DIREC from the Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis.

References Aguiar, L.M.S., Machado, R.B., Zortéa, M., Mendes, S.L., and Rylands, A.B. 1998. Working with the IUCN Red List categories: the experience of the Workshop on the Conservation of Brazilian Bats. Bol. Mus. Biol. Mello Leitao (N.S), 9: 3–11. Albernaz, A.K.L.M. 2002. Zoneamento da região de Alter do Chão, Pará : um exercício de planejamento para uma Unidade de Conservação de Uso Direto. Ph.D. thesis, Instituto Nacional de Pesquisas da Amazônia, Manaus, Brazil. Aldridge, H.D.J.N., and Rautenbach, I.L. 1987. Morphology, echolocation and resource partitioning in insectivorous bats. J. Anim. Ecol. 56: 763–778. Altringham, J.D. 1996. Bats—biology and behaviour. Oxford University Press, Oxford. Ascorra, C.F., Gorchov, D.L., and Cornejo, F. 1993. The bats from Jenaro Herrera, Loreto, Peru. Mammalia, 57: 533–552. Ascorra, C.F., Solari, S., and Wilson, D.E. 1996. Diversidad y ecologia de los quirópteros en Pakitza. In Manu: the biodiversity of southern Peru. Edited by D.E Wilson and A. Sandoval. Editora Horizonte, Lima, Peru. pp. 593–612. Bernard, E. 1997. Folivory in Artibeus concolor (Chiroptera: Phyllostomidae): a new evidence. Chiroptera Neotrop. 3: 77–79. Bernard, E. 2001a. Species list of bats (Mammalia: Chiroptera) of Santarém area, Pará State, Brazil. Rev. Bras. Zool. 18: 455–463. Bernard, E. 2001b. First capture of Micronycteris homezi Pirlot (Chiroptera: Phyllostomidae) in Brazil. Rev. Bras. Zool. 18: 645– 647. Bernard, E. 2001c. Vertical stratification of bat communities in primary forests of central Amazon, Brazil. J. Trop. Ecol. 17: 115–126. Bernard, E. 2002. Diet, activity and reproduction of bat species (Mammalia: Chiroptera) in central Amazonia, Brazil. Rev. Bras. Zool. 19: 173–188. Bernard, E., Albernaz, A.L.K.M., and Magnusson, W.E. 2001. Bat species composition in three sites in the Amazon Basin. Stud. Neotrop. Fauna Environ. 36: 177–184. Brosset, A., and Charles-Dominique, P. 1990. The bats from French Guiana: a taxonomic, faunistic and ecological approach. Mammalia, 54: 509–560. Bunge, J., and Fitzpatrick, M. 1993. Estimating the number of species: a review. J. Am. Stat. Assoc. 88: 364–373. Chao, A. 1984. Non-parametric estimation of the number of classes in a population. Scand. J. Stat. 11: 265–270. Chao, A. 1987. Estimating the population size for capture–recapture data with unequal catchability. Biometrics, 43: 783–791. Chao, A., Ma, M.C., and Yang, M.C.K. 1993. Stopping rules and estimation for recapture debugging with unequal failure rates. Biometrika, 80: 193–201. Clark, B.S., Leslie, D.M., and Carter, T.S. 1993. Foraging activity of adult female big-eared bats (Plecotus townsendii) in summer. J. Mammal. 74: 422–427. Colwell, R.K. 1997. EstimateS: statistical estimation of species richness and shared species from samples: user’s guide and application. Available at http://viceroy.eeb.uconn.edu/estimates (accessed on 10 March 2002).

Can. J. Zool. Vol. 80, 2002 Colwell, R.K., and Coddington, J.A. 1996. Estimating terrestrial biodiversity through extrapolation. In Biodiversity: measurement and estimation. Edited by D.L. Hawksworth. Chapman and Hall, London. pp. 101–118. Cosson, J.F., Pons, J.M., and Masson, D. 1999. Effects of forest fragmentation on frugivorous and necatrivorous bats in French Guiana. J. Trop. Ecol. 15: 515–534. Daly, D.C., and Prance, G.T. 1989. Brazilian Amazon. In Floristic inventory of tropical countries: the status of plant systematics, collections, and vegetation, plus recommendations for the future. Edited by D.G. Campbell and H.D. Hammond. New York Botanical Garden, New York. pp. 401–426. Ditchfield, A.D. 2000. The comparative phylogeography of Neotropical mammals: patterns of intraspecific mitochondrial DNA variation among bats contrasted to nonvolant small mammals. Mol. Ecol. 9: 1307–1318. Eastmann, J.R. 1995. Idrisi for Windows. Clark Laboratories for Cartographic Technology and Geographic Analysis, Worcester, Mass. Emmons, L.H. 1984. Geographic variation in densities and diversities of non-flying mammals in Amazonia. Biotropica, 16: 210– 222. Emmons, L.H., and Feer, F. 1997. Neotropical rainforest mammals: a field guide. 2nd ed. University of Chicago Press, Chicago. Environmental Systems Research Institute, Inc. 1996. ArcView GIS, version 3.1. Environmental Systems Research Institute, Inc. Redlands, Calif. Fenton, M.B. 1994. Echolocation: its impact on the behaviour and ecology of bats. Ecoscience, 1: 21–30. Fenton, M.B. 1997. Science and conservation of bats. J. Mammal. 78: 1–14. Fenton, M.B., Portfors, C.V., Rautenbach, I.L., and Waterman, J.M. 1998. Compromises: sound frequencies used in echolocation by aerial-feeding bats. Can. J. Zool. 76: 1174–1182. Findley, J.S. 1993. Bats: a community perspective. Cambridge University Press, Cambridge. Fleming, T.H. 1988. The short tailed fruit bat: a study in plant– animal interactions. University of Chicago Press, Chicago. Gascon, C., Malcolm, J.R., Patton, J.L., Silva, M.N.F., Bogart, J.P., Lougheed, S.C., Peres, C.A., Neckel, S., and Boag, P.T. 2000. Riverine barriers and the geographic distribution of Amazonian species. Proc. Natl. Acad. Sci. U.S.A. 97: 13672–13677. Gregorin, R. 1998. Notes on geographic distribution of Neoplatymops mattogrossensis (Vierira, 1942) (Chiroptera: Molossidae). Chiroptera Neotrop. 4: 88–90. Gregorin, R., and Taddei, V.A. 2000. New records of Molossus and Promops from Brazil (Chiroptera: Molossidae). Mammalia, 64: 471–476. Gribel, R., and Taddei, V.A. 1989. Notes on the distribution of Tonatia schulzi and Tonatia carrikeri in the Brazilian Amazon. J. Mammal. 70: 871–873. Gribel. R., Gibbs, P.E., and Queiroz, A.L. 1999. Flowering and pollination of Ceiba petandra (Bombacaceae) in central Amazonia. J. Trop. Ecol. 15: 247–263. Handley, C.O. 1967. Bats of the canopy of an Amazonian forest. Atas Simp. Biota Amazonica (Zool.), 5: 211–215. Handley, C.O., Wilson, D.E., and Gardner, A.L. 1991. Demography and natural history of the common fruit bat Artibeus jamaicensis on Barro Colorado Island, Panamá. Smithson. Contrib. Zool. 511: 1–173. Hutson, A.M., Mickleburgh, S.P., and Racey, P.A. 2001. Microchiropteran bats: global status survey and conservation action plan. IUCN/SSC Chiroptera Specialist Group, International Union © 2002 NRC Canada

J:\cjz\cjz8006\Z02-094.vp Friday, June 28, 2002 2:40:04 PM

Color profile: Disabled Composite Default screen

Bernard and Fenton for the Conservation of Nature and Natural Resources, Gland, Switzerland, and Cambridge, U.K. Jong, J. de. 1994. Habitat use, home range and activity pattern of the northern bat, Eptesicus nilssoni, in a hemiboreal forest. Mammalia, 58: 535–548. Kalko, E.K.V. 1995. Echolocation signal design, foraging habitats and guild structure in six Neotropical sheath-tailed bats (Emballonuridae). Symp. Zool. Soc. Lond. No. 67. pp. 259–273. Kalko, E.K.V., Handley, C.O., and Handley, D. 1996. Organization, diversity, and long-term dynamics of a Neotropical bat community. In Long-term studies of vertebrate communities. Edited by M.L. Cody and J.A. Smallwood. Academic Press, San Diego. pp. 503–553. Kalko, E.K.V., Schnitzler, H.U., Kaipf, I., and Gunnell, A.D. 1998. Echolocation and foraging behaviour of the lesser bulldog bat, Noctilio albiventris: preadaptations for piscivory? Behav. Ecol. Sociobiol. 42: 305–319. Kalko, E.K.V., Friemel, D., Handley, C.O., and Schnitzler, H.U. 1999. Roosting and foraging behavior of two Neotropical gleaning bats, Tonatia silvicola and Trachops cirrhosus (Phyllostomidae). Biotropica, 31: 344–353. Koopman, K.F. 1993. Order Chiroptera. In Mammals species of the world: a taxonomic and geographic reference. 2nd ed. Edited by D.E. Wilson and D.M. Reeder. Smithsonian Institution Press, Washington, D.C. pp. 137–241. Kunz, T.H., and Kurta, A. 1988. Capture methods and holding devices. In Ecological and behavioral methods for the study of bats. Edited by T.H. Kunz. Smithsonian Institution Press, Washington, D.C. pp. 1–29. Kurta, A., and Lehr, G.C. 1995. Lasiurus ega. Mamm. Species No. 515. pp. 1–7. Laurance, W.F., Cochrane, M.A., Bergen, S., Fearnside, P.M., Delamonica, P., Barber, C., D’Angelo, S., and Fernandes, T. 2001. The future of the Brazilian Amazon. Science (Washington, D.C.), 291(5503): 438–439. Law, B.S., and Lean, M. 1999. Common blossom bats (Syconycteris australis) as pollinators in fragmented Australian tropical rainforest. Biol. Conserv. 91: 201–212. Lim, B.K., and Engstrom, M.D. 2001a. Bat community structure at Iwokrama forest, Guyana. J. Trop. Ecol. 17: 647–665. Lim, B.K., and Engstrom, M.D. 2001b. Species diversity of bats (Mammalia: Chiroptera) in Iwokrama Forest, Guyana, and the Guianan subregion: implications for conservation. Biodivers. Conserv. 10: 613–657. Longino, J.T., and Colwell, R.K. 1997. Biodiversity assessment using structured inventory: capturing the ant fauna of a tropical rain forest. Ecol. Appl. 7: 1263–1277. Magnusson, W.E., Araujo, M.C., Cintra, R., Lima, A.P., Martinelli, L.A., Sanaiotti, T.M., Vasconcelos, H.L., and Victoria, R.L. 1999. Contributions of C3 and C4 plants to higher trophic levels in an Amazonian savanna. Oecologia, 119: 91–96. Marinho-Filho, J., and Sazima, I. 1998. Brazilian bats and conservation biology: a first survey. In Bat biology and conservation. Edited by T.H. Kunz and P.A. Racey. Smithsonian Institution Press, Washington, D.C. pp. 282–294. Marques, S.A. 1986. Activity cycle, feeding, and reproduction of Molossus ater (Chiroptera: Molossidae) in Brazil. Bol. Mus. Para. Emilio Goeldi Nova Ser. Zool. No. 2. pp. 159–180. McAleece, N. 1997. Biodiversity professional. The Natural History Museum and The Scottish Association for Marine Science, Oban, Scotland. Miranda, I.S. 1993. Estrutura do estrato arbóreo do cerrado amazônico em Alter do Chão, Pará, Brasil. Rev. Bras. Bot. 16: 143–150.

1135 Mok, W.Y., Wilson, D.E., Lacey, L.A., and Luizão, R.C.C. 1982. Lista atualizada de quirópteros da Amazônia Brasileira. Acta Amazonica, 12: 817–823. Moreno, C.E., and Halffter, G. 2000. Assessing the completeness of bat biodiversity inventories using species accumulation curves. J. Appl. Ecol. 37: 149–158. Norberg, U.M., and Rayner, J.M.V. 1987. Ecological morphology and flight in bats (Mammalia: Chiroptera)—wing adaptations, flight performance, foraging strategy and echolocation. Philos. Trans. R. Soc. Lond. B Biol. Sci. 316: 337–419. Ochoa G.J., O’Farrell, M.J., and Miller, B.W. 2000. Contribution of acoustic methods to the study of insectivorous bat diversity in protected areas from northern Venezuela. Acta Chiropterol. 2: 171–183. O’Farrell, M.J., and Miller, B.W. 1997. A new examination of echolocation calls of some Neotropical bats (Emballonuridae and Mormoopidae). J. Mammal. 78: 954–963. O’Farrell, M.J., and Miller, B.W. 1999. Use of vocal signatures for inventory of free-flying Neotropical bats. Biotropica, 31: 507– 516. Patton, J.L., Silva, M.N.F., and Malcolm, J.R. 2000. Mammals of the Rio Juruá and the evolutionary and ecological diversification of Amazonia. Bull. Am. Mus. Nat. Hist. 244: 1–306. Peres, C.A. 1997. Primate community structure in twenty western Amazonian flooded and un-flooded forests. J. Trop. Ecol. 13: 381–405. Piccinini, R.S. 1974. Lista provisória dos quirópteros da coleção do Museu Paraense Emilio Goeldi (Chiroptera). Bol. Mus. Para. Emilio Goeldi Nova Ser. Zool. 77: 1–32. Pine, R.H. 1993. A new species of Thyroptera Spix (Mammalia: Chiroptera: Thyropteridae) from the Amazon Basin of northeastern Perú. Mammalia, 57: 213–225. Pires, J.M., and Prance, G.T. 1985. The vegetation types of the Brazilian Amazon. In Amazonia. Edited by G.T. Prance and T.E. Lovejoy. Pergamon Press, Oxford. pp. 109–145. Puhakka, M., and Kalliola, R. 1995. Floodplain vegetation mosaics in western Amazonia. Biogeographica, 71: 1–14. Rautenbach, I.L., Fenton, M.B., and Whiting, M.J. 1996. Bats in riverine forest and woodlands: a latitudinal transect in southern Africa. Can. J. Zool. 74: 312–322. Reid, F.A., Engstrom, M.D., and Lim, B.K. 2000. Noteworthy records of bats from Ecuador. Acta Chiropterol. 2: 37–51. Reis, N.R. 1984. Estrutura de comunidades de morcegos na região de Manaus, Amazonas. Rev. Bras. Biol. 44: 247–254. Reis, N.R., and Guillaumet, J.L. 1983. Les chauve-souris frugivores de la région de Manaus et leur rôle dans la dissémination des espècies végétales. Rev. Ecol. Terre Vie, 38: 149–169. Reis, N.R., and Peracchi, A.L. 1987. Quirópteros da região de Manaus, Amazonas, Brasil (Mammalia, Chiroptera). Bol. Mus. Para. Emilio Goeldi Nova Ser. Zool. 3: 161–182. Reis, N.R., and Schubart, H.O.R. 1979. Notas preliminares sobre os morcegos do Parque Nacional da Amazonia (Médio Tapajós). Acta Amazonica, 9: 507–515. Robinson, M.F., and Stebbings, R.E. 1997. Home range and habitat use by the serotine bat, Eptesicus serotinus, in England. J. Zool. (Lond.), 243: 117–136. Rylands, A.B., and Pinto, L.P.S. 1998. Conservação da Biodiversidade na Amazônia Brasileira : uma análise do sistema de unidades de conservação. Cad. Fund. Bras. Desenvolv. Sustentavel, 1: 14–15. Sampaio, E.M. 2000. Effects of forest fragmentation on the diversity and abundance patterns of central Amazonian bats. Ph.D. thesis, University of Tübingen, Tübingen, Germany, and LogosVerlag, Berlin. © 2002 NRC Canada

J:\cjz\cjz8006\Z02-094.vp Friday, June 28, 2002 2:40:05 PM

Color profile: Disabled Composite Default screen

1136 Sampaio, E.M., Kalko, E.K.V., Bernard, E., Herrera, B., and Handley, C.O. 2002. A biodiversity assessment of bats (Chiroptera) in an upland rainforest in central Amazonia including methodological and conservation considerations. Stud. Neotrop. Fauna Environ. In press. Simmons, N.B., and Handley, C.O. 1998. A revision of Centronycteris Gray (Chiroptera: Emballonuridae) with notes on natural history. Am. Mus. Novit. No. 3239. pp. 1–28. Simmons, N.B., and Voss, R.S. 1998. The mammals of Paracou, French Guiana: a Neotropical lowland rainforest fauna. Part I. Bats. Bull. Am. Mus. Nat. Hist. 237. Simmons, N.B., Voss, R.S., and Peckham, H.C. 2000. The bat fauna of Säul region, French Guiana. Acta Chiropterol. 2: 23–36. StatSoft Inc. 1998. Statistica for Windows, version 5.1. StatSoft Inc. Tulsa, Okla. Taddei, V.A., and Reis, N.R. 1980. Notas sobre alguns morcegos da Ilha de Maracá, Território Federal de Roraima (Mammalia: Chiroptera). Acta Amazonica, 10: 363–368. Thomas, O. 1901. New species of Saccopteryx, Sciurus, Rhipidomis, and Tatu from South America. Ann. Mag. Nat. Hist. 7: 366–371. Tuomisto, H., Linna, A., and Kalliola, R. 1994. Use of digital processed satellite images in studies of tropical rain forest vegetation. Int. J. Remote Sens. 15: 1595–1610.

Can. J. Zool. Vol. 80, 2002 Uieda, W. 1980. Ocorrência de Carollia castanea na Amazônia Brasileira (Chiroptera: Phyllostomidae). Acta Amazonica, 10: 936–938. Uieda, W., and Vasconcellos-Neto, J. 1985. Dispersão de Solanum spp. (Solanaceae) por morcegos na região de Manaus, Amazonas, Brasil. Rev. Bras. Zool. 2: 449–458. Vonhof, M.J. 2001. Habitat availability, population size, and the composition, stability, and genetic structure of social groups of Spix’s disk-winged bat, Thyroptera tricolor. Ph.D. thesis, York University, Toronto, Ont. Voss, R.S., and Emmons, L.H. 1996. Mammalian diversity in Neotropical lowland rainforests: a preliminary assessment. Bull. Am. Mus. Nat. Hist. 230. Voss, R.S., Lunde, D.P., and Simmons, N.B. 2001. The mammals of Paracou, French Guiana: a Neotropical lowland rainforest fauna. Part 2: Nonvolant species. Bull. Am. Mus. Nat. Hist. 263. Whitmore, T.C. 1997. Tropical forest disturbance, disappearance, and species loss. In Tropical forest remnants: ecology, management, and conservation of fragmented communities. Edited by W.F. Laurance and R.O. Bierregaard. University of Chicago Press, Chicago. pp. 3–12.

© 2002 NRC Canada

J:\cjz\cjz8006\Z02-094.vp Friday, June 28, 2002 2:40:05 PM

Color profile: Disabled Composite Default screen

Bernard and Fenton

1137

Appendix A Table A1. Bat species reported at 18 Neotropical sites: 1, Montes Azules, México; 2, La Selva, Costa Rica; 3, Barro Colorado Island, Panamá; 4, Imataca, Venezuela; 5, Piste St. Élie, French Guiana; 6, Paracou, French Guiana; 7, Arataye, French Guiana; 8, Cunucunuma, Venezuela; 9, Manaus, Brazil; 10, Jenaro Herrera, Perú; 11, Balta, Perú; 12, Manú, Perú; 13, Cuzco Amazônico, Perú; 14, Iwokrama Forest, Guyana; 15, San Juan de Manapiare, Venezuela; 16, Yasuni, Ecuador; 17, Säul, French Guiana; 18, Alter do Chão, Brazil. See the text for references.

Locality B. plicata B. io C. centralis C. maximiliani C. brevirostris C. alecto D. albus D. ingens D. isabelus D. scutatus P. kappleri P. leucoptera P. macrotis P. trinitatis R. naso S. bilineata S. canescens S. gymnura S. leptura N. albiventris N. leporinus M. megalophylla P. davyi P. gymnonotus P. parnellii P. personatus D. rotundus D. youngi D. ecaudata A. caudifera A. cultrata A. geoffroy A. latidens A. sp. nov. C. godmani C. minor G. commissarisi G. longirostris G. soricina H. underwoodi L. obscura L. spurelli L. mordax L. robusta L. thomasi

1 1 1 0 0 0 0 0 0 0 0 1 0 1 0 1 1 0 0 0 1 1 1 1 1 1 0 1 1 1 0 0 0 0 0 0 0 1 0 1 1 0 0 0 0 0

2 0 0 1 0 1 1 1 0 0 0 1 0 0 0 1 1 0 0 1 1 1 0 1 0 1 0 1 0 0 0 0 0 0 0 1 0 1 0 1 1 1 0 0 1 0

3 0 0 1 0 1 0 1 0 0 0 0 0 0 0 1 1 0 0 1 1 1 0 0 1 1 0 1 0 0 0 0 0 0 0 0 0 1 0 1 0 0 0 0 1 0

4 0 0 0 0 1 0 1 0 0 1 1 0 1 0 1 1 1 0 1 1 1 0 0 0 1 0 1 0 0 0 0 1 1 0 1 1 0 0 1 0 1 1 0 0 1

5 0 0 0 0 1 1 0 0 0 0 0 1 1 0 0 1 0 0 1 0 0 0 0 0 0 0 1 0 0 1 0 0 0 0 0 1 0 0 1 0 0 1 0 0 1

6 0 0 0 1 1 0 0 0 0 1 1 1 1 0 1 1 0 1 1 1 1 1 0 0 1 0 1 1 0 1 0 0 0 0 0 1 0 0 1 0 1 0 0 0 1

7 0 0 0 0 1 0 0 0 0 1 0 0 1 0 0 1 0 0 1 0 0 0 0 0 1 0 1 0 0 1 0 1 0 0 0 1 0 0 1 0 1 1 0 0 1

8 0 0 0 0 1 0 0 0 0 0 0 0 1 0 1 1 0 0 1 0 1 0 0 0 1 0 1 0 0 1 0 0 0 0 0 0 0 0 1 0 0 1 0 0 0

9 0 0 0 1 1 0 1 0 0 0 1 1 1 0 1 1 1 1 1 1 1 0 0 1 1 0 1 1 0 1 0 0 0 0 0 1 0 0 1 0 1 1 0 0 1

10 0 0 0 0 0 0 0 0 0 0 1 1 0 0 1 1 0 0 1 1 0 0 0 0 0 0 1 0 0 1 0 0 0 0 0 1 0 0 1 0 0 0 1 0 1

11 12 0 0 0 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 1 0 0 0 0 0 0 1 1 1 1 0 0 0 0 1 1 1 1 0 1 0 0 0 0 0 0 0 0 0 0 1 1 0 0 0 1 1 1 0 1 1 1 0 0 0 1 0 1 1 1 0 1 0 0 1 1 0 0 0 0 0 1 0 0 0 0 1 1

13 0 0 0 0 0 0 0 0 0 0 0 1 0 0 1 1 0 0 1 1 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 1 0 0 1 0 0 0 0 0 1

14 0 0 0 1 1 0 1 1 1 0 0 1 1 0 1 1 1 1 1 1 1 0 0 1 1 1 1 1 0 0 0 1 0 0 0 1 0 0 1 0 0 1 0 0 1

15 0 0 0 0 1 0 1 0 1 1 0 0 1 1 1 1 1 0 1 1 0 0 0 0 1 0 1 1 0 0 0 1 1 0 0 0 0 1 1 0 0 1 0 0 1

16 0 0 0 0 1 0 0 0 0 0 0 0 1 0 1 1 0 0 1 1 1 0 0 0 0 0 1 0 1 1 0 0 0 0 0 1 0 0 1 0 1 0 0 0 1

17 0 0 0 1 1 0 0 0 0 0 0 0 0 0 0 1 0 0 1 0 0 0 0 0 1 0 1 0 0 1 0 0 0 0 0 1 0 0 1 0 0 1 0 0 1

18 0 0 0 0 1 0 0 1 0 0 0 1 1 0 1 1 1 0 0 1 0 0 0 1 1 0 1 0 0 0 0 0 0 0 0 1 0 0 1 0 1 0 0 0 1

© 2002 NRC Canada

J:\cjz\cjz8006\Z02-094.vp Friday, June 28, 2002 2:40:06 PM

Color profile: Disabled Composite Default screen

1138

Can. J. Zool. Vol. 80, 2002 Table A1 (continued).

Locality S. ega C. auritus G. daviesi G. sylvestris L. brachyotis L. aurita L. inusitata M. macrophyllum M. waterhousii M. brosseti M. hirsuta M. homezi M. megalotis M. microtis M. minuta M. schmidtorum M. bennettii M. cozumelae M. crenulatum P. stenops P. discolor P. elongatus P. hastatus P. latifolius T. bidens T. brasiliense T. carrikeri T. evotis T. saurophila T. schulzi T. silvicola T. cirrhosus T. nicefori V. spectrum C. brevicauda C. castanea C. perspicillata C. sp. nov. R. fischerae R. pumilio A. centurio A. amplus A. aztecus A. jamaicensis A. planirostris A. lituratus A. obscurus A. anderseni A. cinereus A. glaucus A. gnomus A. phaeotis

1

2

3

4

5

6

7

8

9

10

0 1 0 0 1 1 0 1 1 0 0 0 1 0 0 1 0 1 1 1 1 0 0 0 0 1 0 1 1 0 0 1 0 0 1 0 1 0 0 0 0 0 1 1 0 1 0 0 0 0 0 1

0 1 1 0 1 0 0 1 0 0 1 0 0 1 1 1 0 1 1 1 1 0 1 0 0 1 0 0 1 0 1 1 1 1 1 1 1 0 0 0 0 0 0 1 0 1 0 0 0 0 0 1

0 1 0 0 1 0 0 1 0 0 1 0 0 1 0 1 0 0 1 1 1 0 1 0 0 1 0 0 1 0 1 1 1 1 1 1 1 0 0 0 1 0 0 1 0 1 0 0 0 0 0 1

0 1 1 0 0 0 1 1 0 0 0 0 1 1 1 0 0 0 1 1 1 1 1 0 0 1 0 0 1 0 1 1 1 1 1 0 1 0 0 1 1 0 0 1 0 1 1 0 1 1 1 0

0 1 1 0 0 0 0 1 0 0 0 0 1 1 1 0 0 0 1 1 1 1 1 0 0 1 0 0 1 1 1 0 1 1 0 0 1 0 0 1 1 0 0 1 0 1 1 0 1 0 1 0

0 1 1 1 0 0 0 1 0 1 1 1 1 1 1 1 1 0 1 1 1 1 1 0 0 1 1 0 1 1 1 1 1 1 0 0 1 0 0 1 1 0 0 1 0 1 1 0 1 0 1 0

0 1 0 1 0 0 1 1 0 0 0 0 1 1 0 0 1 0 1 1 1 1 1 1 0 0 0 0 1 1 1 1 1 1 1 0 1 0 0 1 1 0 0 1 0 1 1 0 0 0 1 0

1 1 0 0 0 0 1 1 0 0 0 0 1 1 0 1 0 0 0 1 0 1 1 0 0 0 0 0 0 0 1 0 0 0 1 0 1 0 0 1 1 1 0 1 0 1 1 0 0 1 1 0

0 1 1 1 1 0 0 1 0 0 1 0 1 0 1 1 0 0 1 1 1 1 1 1 1 1 1 0 1 1 1 1 1 1 1 1 1 0 0 1 1 0 0 1 0 1 1 1 1 0 1 0

0 1 0 0 0 0 0 0 0 1 0 0 1 0 0 0 0 0 1 1 1 1 1 0 0 1 1 0 1 0 1 1 1 1 1 1 1 0 1 1 0 0 0 1 0 1 1 1 0 0 1 0

11 12 0 0 0 0 0 0 0 1 0 0 0 0 1 0 0 0 0 0 1 0 0 1 1 0 0 1 1 0 1 0 1 1 1 0 1 1 1 0 0 1 0 0 0 1 0 1 1 1 1 0 0 0

0 1 0 0 1 0 0 1 0 0 1 0 1 0 1 1 0 0 1 1 0 1 1 0 0 1 0 0 1 0 1 1 0 1 1 1 1 0 0 1 0 0 0 1 0 1 1 1 1 1 1 0

13

14

15

16

17

18

0 1 0 0 0 0 0 0 0 0 0 0 1 0 1 0 0 0 1 0 0 1 1 0 0 0 0 0 0 0 1 1 0 1 1 1 1 1 0 1 0 0 0 1 0 1 1 1 1 0 0 0

0 1 1 1 1 1 0 1 0 0 1 0 1 1 1 0 0 0 1 1 1 1 1 0 0 1 1 0 1 1 1 1 1 1 1 0 1 0 0 1 1 0 0 1 0 1 1 0 1 1 1 0

0 1 0 1 0 0 0 1 0 0 1 0 1 1 1 1 0 0 1 1 1 1 1 0 1 1 1 0 1 0 1 1 1 1 1 0 1 0 0 0 1 0 0 1 0 1 1 0 0 0 1 0

0 1 1 0 0 0 0 1 0 0 1 0 1 0 1 0 0 0 1 1 0 1 1 0 0 0 0 0 1 0 1 1 1 1 1 1 1 0 1 1 0 0 0 1 1 1 1 1 1 0 1 0

0 1 0 1 0 0 1 0 0 1 1 0 1 0 0 0 1 0 1 1 0 1 1 1 0 1 0 0 1 1 1 1 1 1 1 0 1 0 0 1 1 0 0 1 0 1 1 0 1 0 1 0

1 1 1 1 1 0 0 0 0 0 1 1 1 0 1 1 0 0 1 1 1 1 1 0 0 1 1 0 1 1 1 1 1 1 1 0 1 0 1 1 1 0 0 1 0 1 1 1 1 0 1 0

© 2002 NRC Canada

J:\cjz\cjz8006\Z02-094.vp Friday, June 28, 2002 2:40:08 PM

Color profile: Disabled Composite Default screen

Bernard and Fenton

1139

Table A1 (continued).

Locality A. watsoni A. concolor C. senex C. salvini C. trinitatum C. villosum E. alba E. macconnelli E. hartii P. brachycephalus P. dorsalis P. helleri P. infuscus P. lineatus S. toxophyllum S. erythromos S. lilium S. ludovici S. luisi S. magna S. tildae U. bilobatum U. magnirostrum V. bidens V. brocki V. melissa V. nymphea V. pusilla V. caraccioli N. stramineus F. horrens T. discifera T. lavali T. tricolor E. brasiliensis E. chiriquinus E. furinalis E. melanopterus L. atratus L. blossevillii L. ega M. albescens M. elegans M. fortidens M. keaysi M. nigricans M. riparius M. simus P. subflavus R. tumida B. dubiaquercus

1

2

3

4

5

6

7

8

9

10

1 0 1 1 0 1 0 0 0 0 0 1 0 0 0 0 1 1 0 0 0 1 0 0 0 0 0 1 1 1 0 0 0 1 0 0 1 0 0 1 1 1 1 1 1 0 0 0 1 0 1

1 0 0 0 0 1 1 0 0 0 0 1 0 0 0 0 1 1 0 0 0 1 0 0 0 0 1 1 1 0 1 0 0 1 0 1 1 0 0 0 0 1 1 0 0 1 1 0 0 1 0

1 0 1 0 0 1 0 1 1 0 0 1 0 0 0 0 0 0 1 0 0 1 1 0 0 0 1 1 1 1 0 1 0 1 0 0 1 0 0 0 0 1 0 0 0 1 1 0 0 1 0

0 1 0 0 1 1 0 1 0 1 0 1 0 0 0 0 1 0 0 0 1 1 1 1 0 0 0 1 1 0 0 0 0 1 1 1 1 0 1 0 0 0 0 0 0 1 1 0 0 0 0

0 1 0 0 1 1 0 1 0 0 0 1 0 0 0 0 1 0 0 0 1 1 0 0 0 0 0 1 0 0 1 0 0 1 0 1 1 0 0 0 0 0 0 0 0 1 1 0 0 0 0

0 1 0 0 1 1 0 1 0 0 0 1 0 0 0 0 1 0 0 0 1 1 0 0 1 0 0 0 0 0 1 0 0 1 0 1 1 0 0 1 0 0 0 0 0 1 1 0 0 0 0

0 1 0 0 1 1 0 1 0 0 0 1 0 0 0 0 1 0 0 0 1 1 0 0 1 1 0 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 1 1 0 0 0 0

0 1 0 0 1 1 0 1 0 0 0 1 0 0 0 0 1 0 0 0 1 1 0 1 0 0 0 0 1 0 1 0 0 1 1 0 0 0 0 0 0 1 0 0 0 1 0 0 0 0 0

0 1 0 0 1 1 0 1 0 0 0 1 0 0 0 0 1 0 0 0 1 1 1 1 1 0 0 0 0 0 1 1 0 1 1 1 0 1 0 1 0 1 0 0 0 1 1 0 0 0 0

0 1 0 0 1 1 0 1 1 1 0 1 0 0 0 0 1 0 0 1 1 1 1 0 1 0 0 1 0 0 1 1 0 0 1 0 0 0 0 0 0 1 0 0 0 1 1 1 0 0 0

11 12 0 1 0 0 1 1 0 1 0 1 0 1 1 0 0 0 1 0 0 0 1 1 1 1 0 0 0 1 1 0 0 0 0 1 1 0 1 0 0 1 1 1 0 0 0 1 1 1 0 0 0

0 0 0 1 1 1 0 1 1 1 1 1 1 1 1 1 1 0 0 1 1 1 1 1 0 1 0 1 1 0 1 0 0 1 1 0 1 0 0 0 1 1 0 0 1 1 1 1 0 0 0

13

14

15

16

17

18

0 0 0 1 0 1 0 1 0 0 0 1 1 0 0 0 1 0 0 0 1 1 1 0 0 0 0 1 0 0 0 0 0 1 1 0 0 0 0 0 1 1 0 0 0 1 1 0 0 0 0

0 1 0 0 1 1 0 1 0 0 0 1 0 0 0 0 1 0 0 0 1 1 0 1 1 0 0 1 1 0 0 0 0 1 1 0 0 0 1 1 0 1 0 0 0 1 0 0 0 0 0

0 1 0 0 1 1 0 1 1 0 0 1 0 0 1 0 1 0 0 0 0 1 1 1 0 0 0 0 1 0 0 0 0 0 1 0 1 0 0 1 1 1 0 0 0 0 0 0 0 0 0

0 0 0 0 1 1 0 1 0 1 0 1 1 0 0 0 1 0 0 1 1 1 0 1 0 0 0 1 1 0 1 0 1 1 1 0 0 0 0 0 0 0 0 0 0 1 1 0 0 0 0

0 0 0 0 0 0 0 0 0 0 0 1 0 0 0 0 1 0 0 0 1 1 0 0 0 0 0 0 1 0 1 0 0 1 0 0 1 0 1 0 0 0 0 0 0 0 1 0 0 0 0

0 1 0 0 1 1 0 1 0 1 0 1 0 0 0 0 1 0 0 0 1 1 1 1 0 0 0 0 0 0 0 0 1 1 1 1 0 0 0 1 0 1 0 0 0 0 1 0 0 0 0

© 2002 NRC Canada

J:\cjz\cjz8006\Z02-094.vp Friday, June 28, 2002 2:40:09 PM

Color profile: Disabled Composite Default screen

1140

Can. J. Zool. Vol. 80, 2002

Table A1 (concluded).

Locality E. auripendulus E. bonariensis E. glaucinus E. hansae E. maurus E. trumbulli M. abrasus M. aztecus M. greenhalli M. paranus M. planirostris M. neglectus M. barnesi M. bondae M. coibensis M. molossus M. rufus M. sinalaoe M. temminckii N. matogrossensis N. macrotis N. laticaudatus P. centralis P. nasutus

1 0 0 0 1 0 0 0 0 1 0 0 0 0 0 0 1 1 0 0 0 0 0 0 0

2 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 0 0 1 0 0 0 0 0 0

3 1 0 0 0 0 0 0 0 0 0 0 0 0 1 1 1 0 1 0 0 0 1 0 0

4 1 0 0 1 0 0 1 0 1 1 0 1 0 0 0 1 1 0 0 0 0 1 0 0

5 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 1 0 0 0 0 0 0 0

6 1 0 0 1 0 0 1 0 0 1 0 0 1 0 0 1 1 1 0 0 0 0 1 0

7 0 0 0 1 0 0 0 0 1 1 1 0 0 0 0 1 1 0 0 0 0 1 0 0

8 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 1 0 0 0 0 1 0 0

9 0 0 0 0 0 1 1 0 1 0 0 0 0 1 0 1 1 0 0 0 0 0 0 0

10 0 0 0 0 0 0 0 0 0 0 0 1 0 0 0 1 1 0 0 0 0 0 1 0

11 12 0 0 0 0 0 0 0 0 0 0 0 0 1 0 1 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 1 1 0 0 0 0 0 0 0 0 0 0 0 1 0 0 0 0

13 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0

14 1 0 0 1 0 0 1 0 0 1 0 1 0 0 0 1 1 0 0 0 1 0 0 0

15 0 0 1 1 0 0 0 0 0 0 1 0 0 0 0 1 1 0 0 0 0 0 0 1

16 1 0 0 1 1 0 0 0 0 1 0 0 0 0 1 1 1 0 1 0 0 0 1 0

17 1 0 0 1 0 0 0 0 0 0 1 0 0 0 0 1 1 0 0 0 0 0 0 0

18 0 1 0 0 0 0 0 0 0 1 1 0 0 0 0 1 0 0 1 0 0 0 0 0

© 2002 NRC Canada

J:\cjz\cjz8006\Z02-094.vp Friday, June 28, 2002 2:40:10 PM