Bats of Jaú National Park, central Amazônia, Brazil
Author(s): Adrian A. Barnett , Erica M. Sampaio , Elisabeth K. V. Kalko ,
Rebecca L. Shapley , Erich Fischer , George Camargo , and Bernal RodríguezHerrera
Source: Acta Chiropterologica, 8(1):103-128. 2006.
Published By: Museum and Institute of Zoology, Polish Academy of Sciences
DOI: http://dx.doi.org/10.3161/1733-5329(2006)8[103:BOJNPC]2.0.CO;2
URL: http://www.bioone.org/doi/
full/10.3161/1733-5329%282006%298%5B103%3ABOJNPC%5D2.0.CO%3B2
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Acta Chiropterologica, 8(1): 103–128, 2006
PL ISSN 1508-1109 © Museum and Institute of Zoology PAS
Bats of Jaú National Park, central Amazônia, Brazil
ADRIAN A. BARNETT1, 2, ERICA M. SAMPAIO3, ELISABETH K. V. KALKO3, 4, REBECCA L.
SHAPLEY1, ERICH FISCHER5, GEORGE CAMARGO5, and BERNAL RODRÍGUEZ-HERRERA6
1Akodon Ecological Consulting, 951 Bancroft Rd., Suite 111a, Concord, CA 94518, USA
E-mail: adrian@akodon.com
Centre for Research in Evolutionary Anthropology, School of Life Sciences, Roehampton University, London
SW15 3SN, United Kingdom
3
University of Ulm, Department of Experimental Ecology, Germany, and Division of Mammals, Smithsonian
Institution-NMNH, Washington, DC 20560-0108, USA
4
Smithsonian Tropical Research Institute, Balboa, Panamá
5
Departamento de Biologia, Universidade Federal de Mato Grosso do Sul, Campo Grande,
M.S. 79070-900, Brazil
6
Historia Natural, Museo Nacional de Costa Rica, 749-1000, San José, Costa Rica
2
Although recognized as highly diverse, the bat fauna of the Amazon basin has been only patchily sampled. This
paper combines data from five short surveys conducted between 1998 and 2001 in Jaú National Park, 220 km
east of Manaus, central Amazônia. We used mist-nets, recordings of echolocation calls and roost visits to
provide the first bat inventory for this area. A total of 53 bat species in 33 genera and five families were
documented, including several species that are regarded as rare, in particular Saccopteryx gymnura,
Vampyriscus brocki, Molossops neglectus, and Promops centralis. The Chao 1 index indicates that sampling is
about 72% complete, suggesting that around 73 bat species might co-exist in Jaú. We compare the composition
of Jaú’s bat fauna to those of other sites in Amazônia and interpret the resulting patterns of diversity. Data on
reproduction are given for 14 species.
Key words: Amazônia, inventory, bats, ecology, conservation
INTRODUCTION
Neotropical bat communities are highly
diverse and provide important ecosystem
services including seed dispersal (e.g.,
Galindo-González, 1998; Gastal and Bizerril, 1999; Lobova et al., 2003) and pollination (e.g., Fleming et al., 1996; Helversen
and Winter, 2003; Tschapka, 2003) for up to
a quarter of all trees in some forest communities as well as predation on a large number
of arthropods (e.g., Findley, 1993; Kalka
and Kalko, 2006). Hence, a better understanding of species composition and diversity patterns of bats is of central interest in
community ecology and conservation.
Central Amazônia has been the focus of
a suite of bat studies (e.g., Handley, 1967;
Reis and Guillaumet, 1983; Reis, 1984;
Uieda and Vasconcellos-Neto, 1985; Reis
and Peracchi, 1987; Gribel and Taddei,
1989; Marinho-Filho and VasconcellosNeto, 1994; Gribel et al., 1999; Bernard,
2001a, 2001b, 2002; Kalko and Handley,
104
A. A. Barnett, E. M. Sampaio, E. K. V. Kalko, R. L. Shapley, E. Fischer, et al.
2001; Bernard and Fenton, 2003; Sampaio
et al., 2003). Almost without exception,
these were focused on sites within 100 km
of Manaus, Brazil, the Amazonas’ state capital. These studies show, as for many other
taxa, that diversity patterns and community
composition of bats may vary over quite
short distances, and this can have important
consequences for conservation as it may require different management strategies even
in seemingly homogeneous areas (Wilson,
1996; Sampaio et al., 2003).
One of the principal goals of conservationists is to preserve the species-rich habitats of the Amazon basin (e.g., Kress et al.,
1998). Local inventories in central Amazônia, even if they are only short-term, increase our knowledge of the local fauna
through a preliminary characterization of
species composition and relative abundance. They also add more detail to the
known distribution of species and often provide new localities for rare species.
Here we report the results of five short
surveys of the bat fauna of Jaú National Park, western Amazonas state, Brazil,
which were conducted between 1998 and
2001. The fauna and flora of Jaú is currently
studied through the ‘Windows of Biodiversity’ research program. Coordinated
by Fundaçno Vitória Amazônica (FVA),
a Manaus-based NGO, and IBAMA (Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis), this program
has already resulted in a number of detailed
botanical and zoological inventories (see
Ferreira, 1997, 1999; Borges and Carvalhaes, 2000; Motta and Andreazze, 2001; Barnett et al., 2002, 2005). General distribution
maps published in field guides (Emmons
and Feer, 1997; Eisenberg and Redford,
1999) and national checklists (MarinhoFilho and Sazima, 1998) indicate that the
Jaú region has a rich and diverse bat fauna,
but there have been no published studies
of the bats of the national park, nor the
surrounding area. Gribel and Taddei (1989)
reported sampling bats in the Jaú region, but
did not provide a list of species. Taken together, the surveys we report upon here provide the first, albeit preliminary, inventory
of the bats of the Jaú river basin.
MATERIALS AND METHODS
Site Description
Jaú National Park covers 2,272,000 ha. Encompassing the entire drainage basin of the Jaú river,
the park is located on the left bank of the Río Negro some 220 km upstream from Manaus, Brazil
(Fig. 1, locality 4). Elevation varies between 50–100
m a.s.l., with a small area of sub-montane forest at
200–300 m a.s.l. (S. Borges, personal comm.). The
grid reference for the mouth of the Jaú river is
01°50’S, 62°50’W. The human population density in
the Jaú drainage basin is very low, being only one
quarter of the 1.6 persons/km2 that constitutes the average human density in rural Amazônia (Chapman
and Peres, 2001). Terrestrial habitats mainly include
unflooded lowland rainforest (terra firme, ca. 85%),
with some seasonally-flooded blackwater swamps
(igapó, 12%), a few white-sand vegetation types
(campina, campinarana, 2%), and a few other habitat
types (ca. 1% of Jaú’s area). These minor habitats include beaches (capoeira), swamps with Mauritia
palms (buritizal) and giant Montrichardia aroids
(aningal), as well as land used by humans for slashand-burn agriculture (S. Borges, personal comm.).
Monthly temperature means range between 26.3 and
27.2°C and mean total annual precipitation varies between 1,760 and 2,500 mm. The rainy season lasts
from November to May, and there is a marked dry
season from June to September (Ferreira and Prance,
1999). Peak rains are in March (325 mm), while
August is the driest month (30 mm; Ferreira, 1997).
Gazetteered in 1990, Jaú National Park is jointly managed by FVA and IBAMA, and is Brazil’s secondlargest rainforest national park after the Mountains of
Tumucumaque National Park, created in 2002.
Between 1998 and 2001, five surveys of Jaú’s
bats were conducted during four visits to the national
park: two surveys in 1998 focusing on white-sand
vegetation; one survey in 1998 with the main focus on
igapó and beach vegetation; and two surveys, one
in 2000 and another one in 2001, which sampled
terra firme habitats, igapó, and habitats created by
slash-and-burn agriculture. Methodologies are described individually because different sampling methods were used from survey to survey (Table 1).
Bats of Jaú National Park in Brazil
Taxonomy follows Simmons (2005), who recognizes
the genus Lophostoma for L. brasiliense, L. carrikeri,
L. evotis, L. silvicolum and L. schulzi (Lee et al.,
2002), previously included in Tonatia. Simmons
(2005) also lists Mesophylla macconnelli as Mesophylla following Baker et al. (2000), and not as Ectophylla (Simmons and Voss, 1998; Wetterer et al.,
2000) or Vampyressa (Owen, 1987). Furthermore, we
follow Baker et al. (2000) and Wetterer et al. (2000),
and adopt Dermanura as a subgenus of Artibeus for
Artibeus anderseni, A. aztecus, A. cinereus, A. glaucus, A. gnomus, A. incomitatus, A. phaeotis, and
A. watsoni. We also followed Lim et al. (2004) and
used Artibeus jamaicensis, distinct from A. planirostris, for our samples from Jaú, and adhered
to Porter and Baker (2004) who separated the genus Vampyressa into Vampyriscus for V. bidens and
V. brocki, and Vampyressa for V. melissa, V. nymphea,
V. pusilla, and V. thyone.
Sampaio, used ultrasound recordings of bats for species identification. The Campina do Patauá section of
the Jaú National Park is covered by three vegetation
types: campina, campinarana alta, and campinarana
baixa. Campina vegetation is characterized by extensive areas of small, slow-growing bushes and trees up
to 4 m in height, primarily Humiria (Humiriaceae)
and Cyrilla racemosa (Cyrillaceae). Campina is also
known as ‘bana’ or ‘low caatinga’. It is dominated by
Pradosia schomburgkiana (Sapotaceae), Macrolobium canaliculatum (Fabaceae: Caesalpinioideae),
Dimorphandra vernicosa (Fabaceae: Papilionoideae),
and Gongylolepis martiana (Asteraceae: Mutisieae).
The most common habitat in the campina, campinarana baixa, is composed of small trees that are only
up to 6 m tall with rather thin trunks. The less common habitat, campinarana alta, consists of dense but
less diverse stands, with trees up to about 8 m tall. It
is dominated by Aldinia heterophylla (Fabaceae: Papilionoideae). Campinarana is also known as ‘high
caatinga’. For further descriptions of Amazonian
white-sand plant communities, see Anderson (1981)
and Coomes and Grubb (1996).
Surveys in Campina and Campinara
(Campina do Patauá)
Between 28 August and 8 September 1998 (mid/
late dry season), two surveys were made in the white
sand vegetation of the Campina do Patauá, limited by
the Unini and Carabinani rivers (01°49’S, 61°46’W;
altitude 50 m — see Fig. 2, locality 1). One survey,
conducted by Erich Fischer, Juan Gabriel and Bernal Rodríguez-Herrera, involved mist-netting. The
second survey, by B. Rodríguez-Herrera and Erica
80
70
105
Survey in Igapó and Capoeira (Uruá Lake)
Between 15 and 22 November 1998 (late dry season), Enrico Bernard conducted a bat survey with
mist nets in igapó at the mouth of the Jaú river and
around Uruá lake (01°54’S, 61°27’W — see Fig. 2,
locality 2).
60
50
40
10
0
10
FIG. 1. Map showing the location of Jaú and the other sites used for comparison. Peru: 1 — Jenaro Herrera,
2 — Cocha Cashu; Brasil: 3 — Serra do Divisor, 4 — Jaú, 5 — Ilha de Maracá, 6 — BDFFP, 7 — Alter do
Chao, 8 — Xingú river, 9 — Belém; French Guiana: 10 — Saül, 11 — Arataye, 12 — Paracou, 13 —
Sinnamary; Guiana: 14 — Iwokrama forest, 15 — Kanunu mountains; Venezuela: 16 — Imataca, 17 —
Canaima, 18 — Cunucunuma river, 19 — Serrania de los Pijiguaos, 20 — Ticoporo
106
A. A. Barnett, E. M. Sampaio, E. K. V. Kalko, R. L. Shapley, E. Fischer, et al.
Common tree species in the igapó of Jaú include
Amanoa oblongifolia (Euphorbiaceae), Burdacia prismatocapra (Malphigiaceae), Eschweilera tenuifolia
(Lecythidaceae), Macrolobium acaciifolium (Fabaceae: Caesalpiniodeae), Pouteria elegans (Sapotaceae), and Swartzia polyphyla (Fabaceae: Papilionoideae) (Ferreira, 1997, 1999). At mist-netting sites in
igapó, canopy heights varied from 4 to 12 m, and inundation levels ranged from 2 to 6 m. In all cases
there was little mid-level vegetation.
Beach vegetation, or capoeira, was also netted.
The capoeira vegetation rarely exceeded 1 m in height
and included Cuphea balsamina (Lythraceae), Phyllanthus rupestris (Euphorbiaceae), Ishnosiphon sp.
(Marantaceae), Paspalum sp. (Poaceae) and Cyperus sp. (Cyperaceae) as also described in Takeuchi
(1962).
Surveys in Human-modified Habitats
(Seringalzinho Village and Parna)
From 18 October to 11 November 2000 (late dry
season), Rebecca Shapley and Adrian Barnett surveyed bats in human-modified habitats around the village of Seringalzinho (01°50’S, 61°35’W; altitude
60 m — see Fig. 2, locality 3) and in the forests 10 km
upriver from there in the vicinity of a floating research station over water (01°53’S, 61°41’W; altitude
50 m). Nets were set in terra firme, igapó and around
human habitations including buildings and agricultural areas.
Roosts were actively searched for and either netted or visually surveyed, following the technique described in Simmons and Voss (1998). Search sites
included hollow trees, logs, and small caves in rocks.
Following Findley and Wilson (1974) and Simmons
and Voss (1998), stands of Heliconia (Heliconiaceae), Musa (Musaceae) and Phenakospermum (Strelitziaceae) were investigated, in particular for roosting
sucker-footed bats (Thyropteridae) and tent-making
bats (Stenodermatinae). Since tent-making bats are
known to use a much wider range of leaves as roosts
than we specifically surveyed (Kunz and McCracken,
1996) and as some bats, in particular the insectivorous
gleaners of the genus Lophostoma are known to roost
in live termite nests (Dechmann et al., 2004) which
we did not include in our roost survey, we may have
missed some species.
Between 11 and 17 July 2001 (early dry season),
Erich Fischer and George Camargo conducted a survey, primarily to collect bat ectoparasites, near the entrance of the rio Jaú into the rio Carabinani that shortly thereafter debouches into the Río Negro. Surveys
were conducted at five points along about 5 km of
the river. Known locally as ‘Parna’, the area comprises the geographical coordinates 01°54’–01°56’S and
61°25’–61°27’W; altitude 50 m (see Fig. 2, locality
4). Mist nets were placed between unflooded trunks
of igapó trees and between the float supports underneath the administration building of the park headquarters.
Sampling Protocols
We used three net sizes to collect bats (length
× height (in m): 6 × 3, 9 × 3, and 12 × 3), all with
four shelves, and a mesh diameter of 30 mm. Mist
nets were mostly positioned at ground level (0–3 m)
and occasionally in the canopy (15–20 m). We used
a standardized measure for capture rate where one
mist-net hour corresponded to one 12 m net open
for one hour. Specimens were identified using Charles
TABLE 1. Summary of the methods in the five surveys, ‘–’ = not sampled
Survey dates
28 August to
8 September 1998
28 August to
8 September 1998
15 to 22 November
1998
18 October to
11 November 2000
11 and 17 July 2001
Habitat
Methods used
Mist-net effort
campina
campinarana high
caatinga
campina
campinarana
igapó
capoeira
terra firme
igapó
buildings and
agricultural areas
igapó
buildings
ground mist-netting
canopy mist-netting
(15–20 m)
ground acoustic survey
campina: 8,048.6 m2/hours
campinarana: 14,345.6 m2/hours
high caatinga: 4,272.8 m2/hours
–
ground mist-netting
igapó: 16,240 m2/hours
capoeira: 2,240 m2/hours
terra firme: 328 m2/hours
igapó: 464 m2/hours
buildings and agricultural
areas: 1491 m2/hours
total: 2,763 m2 hours
ground mist-netting
roost searches
mist-netting
roost searches
Bats of Jaú National Park in Brazil
Handley’s key to Amazonian bats (E. Sampaio,
E. Kalko, and D. Wilson, unpubl. data). For nomenclature we followed Simmons (2005), Lim et al.
(2004), and Porter and Baker (2004). Voucher specimens were deposited in the mammal’s collection of
the Instituto Nacional de Pesquisas da Amazônia
(INPA) in Manaus, at the time under supervision of
Maria Nazareth Ferreira da Silva, curator of the mammal collection of INPA (Table 2). Reproductive status
was determined following Wilson et al. (1991). We
classified females as pregnant, lactating or nonreproductive. We did not differentiate between adults
and subadults and between reproductive active or
inactive males.
B. Rodríguez-Herrera and E. Sampaio conducted
an acoustic bat survey using a custom-made ultrasound recording device (Animal Physiology, University of Tübingen, Germany). Echolocation calls
were picked up with a condenser microphone (frequency response ± 3 dB between 20 and 120 kHz and
a drop in sensitivity of 0.2 dB/kHz at frequencies
down to 15 kHz and up to 200 kHz), digitised at
a sampling rate of 312.5 kHz, stored in a memory array of 3.3 s real time, and read out as an analogue signal at 1/15th reduced speed onto a Walkman Professional (WM-DC6, Sony). The recordings were
subsequently analysed with a custom-made sound
analysis program (SONA-PC colour spectrogram frequency analyser; B. Waldmann, University of Tübingen, Germany) using a Fast Fourier Transformation
(FFT). The signals were displayed on the monitor as
color sonagrams (400 lines), using 256 points and
a Hanning Window. For species identification, design
FIG. 2. Placement of study sites within Jaú National Park
107
of echolocation calls (limited to search calls) were
compared to an extensive reference call library of
Elisabeth Kalko (unpublished data), based on recordings of identified bats from Manaus (Brazil), Venezuela, Costa Rica, Panamá, and Mexico.
Completeness of Samples and Similarity
To assess completeness of our samples, we applied the nonparametric estimator Chao 1 to our mistnet data as estimator for local species richness.
Because nonparametric estimators rely on the number
of discrete contacts or number of individuals (Chao,
1984, 1987), we excluded records obtained with the
bat detector from analysis and focused on all data
from mist-netting and from the roost searches.
Although Jackknife 1 has been proven to perform
better for bat assemblages in general (E. Sampaio,
unpubl. data), and, in particular, for samples with
about 60% of completeness or more (Brose et al.,
2003), we limited our analysis to Chao 1 to ensure
comparability with other studies because Chao 1 has
been more widely used than Jacknife. To place the
bat fauna of Jaú in a broader biogeographic context, we calculated the Jaccard similarity coefficients
(Magurran, 1988) between Jaú and nineteen other
lowland rainforest sites in the Amazon basin (Fig. 1
and Table 4):
Peru — 1) Jenaro Herrera, departamento Loreto,
on the eastern bank of the Río Ucayali and 140 km
SSW Iquitos (04°55’S, 77°44’W), in Ascorra et al.
(1993); 2) Cocha Cashu (11°54’S, 71°22’W) and
Pakitza (11°57’S, 71°17’W), departamento Madre de
108
A. A. Barnett, E. M. Sampaio, E. K. V. Kalko, R. L. Shapley, E. Fischer, et al.
TABLE 2. Bat species recorded at Jaú National Park. Species order follows Eisenberg and Redford (1999).
Taxonomy follows Simmons (2005), except for Tonatia where we refer to Lee et al. (2002), and Vampyriscus
for V. brocki where we follow Porter and Baker (2004). Abbreviations: C — canopy; U — understory; E —
identified from echolocation call recordings; R — roost; V — visual record; Numbers — number netted; X —
netted, but not counted; cf. — identification to be confirmed; sp. — only identified to genus
Species
Rhynchonycteris naso
Saccopteryx bilineata
S. canescens
S. cf. gymnura
S. leptura
Cormura brevirostris
Centronycteris maximiliani
Diclidurus sp.1
Diclidurus sp.2
Desmodus rotundus
Diaemus youngi
Glossophaga soricina
Glossophaga sp.
Lonchophylla thomasi
Chrotopterus auritus
Micronycteris sp.
Macrophyllum macrophyllum
Lophostoma carrikeri
Tonatia saurophila*
Phyllostomus elongatus
P. hastatus
P. cf. latifolius
Trachops cirrhosus
Carollia brevicauda
C. perspicillata
Carollia sp.
Rhinophylla pumilio
Sturnira tildae
Ametrida centurio
Artibeus anderseni**
A. cinereus
A. concolor
A. jamaicensis
A. lituratus
A. obscurus
Mesophylla macconnelli
Vampyriscus brocki
Noctilio albiventris
N. leporinus
Molossops neglectus
Tadarida/Eumops sp.
Eumops bonariensis
Molossus sp.1
Molossus sp.2
Molossus molossus
Promops centralis
Capoeira Campina Campinarana
Buildings
and
agricultural
land
Igapó
S, 4 U
1
2
1
E
E
E
E
E
E
E, 1 U
E
E
E
1U
1C
Total
Terra
no. of
firme individuals
netted
1U
5
1U
2
3
1
2
1
6
1
5
1
1
1
1 C, 2 U
1
4U
2U
1
2 U, 1
1
3
8
1
1U
X
2
7
4
2
9
3
1
2R
V, R
1 C, 1 U
X
1
9
1
1
7
8
4
X
X
1
1
1U
1U
1C
1
4
X
X
1
X
3 R, X
E
E
E
E, 2
E
E
E
E
E
E
E
E
E
E
1
1
X
2
1
7
1
6
1
7
1
3
1
7
12
7
5
3
1
18
3
4
1
8
1
2
9
6
2
12
1
1
3
2
R
1
Bats of Jaú National Park in Brazil
109
TABLE 2. Continued
Species
Vespertilionidae sp.1
Eptesicus brasiliensis
Lasiurus sp.1
Myotis sp.1
Myotis albescens
M. nigricans
M. riparius
Number of species
Capoeira Campina Campinarana
9
E
E
E
E
E
E
20
Buildings
and
agricultural
land
3U
25
11
Igapó
Total
Terra
no. of
firme individuals
netted
1
1
1
1
2
20
1
1
5
> 149
14
* — originally recorded as Tonatia bidens (Fischer et al., 1998)
** — Artibeus anderseni can only be distinguished from A. cinereus based on skull characters (Davis, 1969; Handley, 1987).
The specimen, determined by B. Rodríguez-Herrera, is number 2671 in the zoological collection at INPA, Manaus
Dios, inventory sites on the northern bank of the Río
Manu, in Voss and Emmons (1996).
Brazil — 3) Serra do Divisor, Acre state
(07°23’S, 73°39’W), in Nogueira et al. (1999); 4) Jaú,
data presented in this paper; 5) Ilha de Maracá,
Rorâima state (03°25’N, 61°40’W), in Robinson
(1998); 6) Biological Dynamic of Forest Fragments
Project (BDFFP), 90 km north of Manaus, Amazonas
state (02°25’S, 59°45’W), in Sampaio et al. (2003);
7) Alter do Chao village, Pará state, on the northern
bank of the rio Tapajós (02°30’S, 54°57’W), in Bernard and Fenton (2002); 8) rio Xingú, Pará state, at
a temporary Smithsonian field station on the eastern
bank of the lower rio Xingú, 52 km SSW from Altamira (03°39’S, 52°22’W), in Voss and Emmons
(1996), Appendix: 8; 9) Belém, Pará state, in forest
sites near the main city, ‘Área de Pesquisas Ecológicas do Guama’ (APEG), and in areas of the ‘Instituto de Pesquisa e Experimentaçno Agropecuarias do
Norte’ (IPEAN), comprising várzea, terra firme, and
igapó forest (02°39’S, 55°38’W), in Kalko and Handley (2001).
French Guiana — 10) Saül, French Guiana samples from Les Eaux Claires, 7 km N Saül (03°37’S,
52°12’W) and data compiled by the authors from previous reports, in Simmons et al. (2000); 11) Lower
Arataye catchment in eastern-central French Guiana,
including data from Les Nourages (04°05’N,
52°40’W) and Saut Pararé (04°02’N, 52°42’W), in
Voss and Emmons (1996), Appendix: 5; 12) Domaine
Experimental Paracou (05°16’N, 52°55’W), administered by the Centre de Coopération Internationale en
Recherche Agronomique pour le Développement
(CIRAD), about 12 km SSE of Sinnamary and 33 km
WNW of Kourou, in Simmons and Voss (1998); 13)
Sinnamary, including litoral region (05°22’N,
52°55’W) and terra firme forest along the road of
Saint-Élie (05°18’N, 53°18’W), in Brosset et al.
(1996).
Guyana — 14) Iwokrama forest, district of Potaro-Siparuni, located in central Guyana (04°40’N,
58°41’W for Iwokrama Field Station), in Lim et al.
(1999), and in Lim and Engstrom (2001a, 2001b); 15)
Kanunu mountains, district of Rupununi, southwestern Guyana, samples are from stations along
the Takutu and Rupununi rivers (03°22’N, 59°30’W
at the base camp in Maipaima creek), in Parker et al.
(1993).
Venezuela — 16) Imataca forest reserve, states
of Delta-Amacuro and Bolívar, samples are from
‘unidad’ V (7°45’N, 61°10’W), in Ochoa (1995); 17)
Canaima National Park, Bolívar state (06°26’–
09°39’N, 62°54’–60°38’W), in Ochoa et al. (1993);
18) Inventories from the villages Culebra (03°39’S,
65°43’W) and Acanana (03°32’S, 65°48’W) on the
Río Cunucunuma, territorio federal do Amazonas,
Venezuela, in Voss and Emmons (1996), Appendix: 6;
19) Ticoporo forest reserve, Barinas state, between
the Michay and Quiú rivers (07°49’–08°10’N,
70°37’–70°55’W) compiled with 20) La Serrania de
Los Pijiguaos, Bolívar state, about 140 km SW of
Caicara del Orinoco, between the Caripo and Suapure
rivers (06°26’–06°32’N, 66°40’–66°46’W), in Ochoa
and Sanchez (1988). We conducted a cluster analysis
with the Jaccard similarity coefficients to compare the
similarity of the bat assemblages across sites (Fig. 3).
RESULTS
A total of 53 bat species were documented during the five inventories (Table
2). Of the 53 species recorded, 36 were captured in ground mist-nets, two species were
110
A. A. Barnett, E. M. Sampaio, E. K. V. Kalko, R. L. Shapley, E. Fischer, et al.
sampled in canopy mist-nets, two species
were documented in roosts, one of them
exclusively, and 15 were identified based
on recordings of their echolocation calls.
Though their distinctness is certain, eight of
these species still need to be identified to
species level (Table 2).
Individual Surveys
With the highest capture effort of 630
mist-net hours (mnh), the 1998 mist-net survey in white-sand vegetation showed the
lowest richness in number of species (40 individuals of 14 bat species). However, the
1998 acoustic part of this survey recorded
calls of 15 types of bats that were not captured in mist-nets during this and most other surveys (Table 2). One recording could
only be identified to family; seven were
identified to genus, and eight to species. For
13 of these 15 species, echolocation calls
were the only method by which the species’
presence was registered in Jaú. In comparison to the first mist-net survey, the 1998
igapó and capoeira study caught twice the
number of individuals (90), and almost
twice as many species (26) in fewer mistnet hours (264 mnh: 232 in igapó; 32 in
capoeira) than the samples in the campina. The 2000 study of terra firme, igapó,
and human habitats registered a total of 31
species. The 2001 study in igapó captured
63 individuals of 13 species in 153.5 net
hours.
Completeness of Samples
We applied the nonparametric estimator
Chao 1 to assess the completeness of our
samples focusing on all data from mist-netting and from the roost searches. The results
FIG. 3. Jaccard cluster analysis (single link) showing the classification of the sampled localities in their fauna
similarity, based on presence-absence data. G — Guiana region; C — central Amazônia; CW — central-western
Amazônia; E — eastern Amazônia; CE — central-eastern Amazônia
Bats of Jaú National Park in Brazil
with Chao 1 suggest that sampling of the
region’s bat fauna is 72% complete, or, in
other words, the Jaú basin has a potential to
hold about 73 bat species.
Reproductive Data
Reproductive data were available from
three surveys (2001, 2000, and 1998 in
Campina do Patauá) where a total of 18 reproductively active females (pregnant, lactating) were netted from 14 species (two
species in 1998, nine species in 2000, and
three species in 2001 — see Table 3). The
small number of individuals caught, the
short sampling times and the fact that the
five surveys covered only the dry season
months between August and November prohibited identification of patterns.
DISCUSSION
Similarity of Jaú Samples with Those of
Other Amazonian Bat Faunas
The Jaccard similarity coefficients
showed the highest faunal similarity of
111
the Jaú fauna with local bat assemblages
sampled in the western parts of the Brazilian Amazon (see Fig. 3 and Table 4), in
particular the surveys conducted in Loreto
state, Peru (Ascorra et al., 1993), in Serra
do Divisor, Acre state, Brazil (Nogueira et
al., 1999), and Manaus, Amazonas state,
Brazil (Sampaio et al., 2003). It decreased
slightly in some eastern localities along
similar latitude, such as Belém, Pará state,
Brazil (Kalko and Handley, 2001) and Alter
do Chao (Bernard and Fenton, 2002).
Similarity continued to decrease throughout
the Guianas, and showed the lowest values
for the northernmost localities, such as
Ticoporo, Barinas state, and Serrania de los
Pitiguaos, Bolivár state, Venezuela (Ochoa
and Sanchez, 1988). Similarity values varied between 44% in Jenaro Herrera, Peru, to
28% in the inventories of Ticoporo and Pitiguaos, Venezuela.
As expected from the Jaccard similarity
coefficient, comparisons were influenced
by the difference in number of species
between Jaú and other localities. Although
the number of shared species was high or
TABLE 3. Reproductive records for bats from Jaú National Park. Abbreviations: L — lactating, P — pregnant,
CY — carrying young
Species
Artibeus cinereus
A. jamaicensis
Carollia perspicillata
C. perspicillata
Lonchophylla thomasi
Molossus molossus
M. molossus
M. molossus
Myotis nigricans
M. riparius
M. riparius
Noctilio albiventris
Phyllostomus discolor
P. hastatus
Rhynchonycteris naso
Saccopteryx canescens
Sturnira tildae
Tonatia saurophila
T. saurophila
Status
L
P
P
CY
L
P
P
newborn
L
L
P
L
L
P
L
L
L
L, CY
L
Date
27 Oct. 00
27 Oct. 00
30 Oct. 00
30 Oct. 00
04 Nov. 00
14 Jun. 01
14 Jun. 01
14 Jun. 01
13 Jun. 01
08 Sep. 98
18 Jun. 01
03 Nov. 00
18 Jun. 01
27 Oct. 00
23 Oct. 00
22 Oct. 00
22 Oct. 00
08 Sep. 98
08 Sep. 98
Season
late dry
late dry
late dry
late dry
late dry
early dry
early dry
early dry
early dry
mid dry
early dry
late dry
early dry
late dry
late dry
late dry
late dry
mid dry
mid dry
112
A. A. Barnett, E. M. Sampaio, E. K. V. Kalko, R. L. Shapley, E. Fischer, et al.
similar to other areas, similarity values were
lower in Jaú in comparison with inventories
of areas with much higher diversity, such as
the Iwokrama forest in Guyana. Although
both areas share a high number of species
(n = 38), the faunal similarity is only 40%
due to the high total number of species from
Iwokrama forest (n = 92).
Calculation of Sample Completeness for Jaú
Calculation of sample coverage by Chao
1 indicates that some 72% of the bat species
of the area have now been recorded with regard to the expected number of species that
may co-exist in the area. To permit accurate
and precise estimation of species richness,
samples should ideally reach between 90 to
95% of sample coverage (see Brose et al.,
2003). Studies have already documented
high numbers of species in other regions of
Amazônia (e.g., Anderson et al., 1982;
Peracchi et al., 1984; Brosset and CharlesDominique, 1990; Simmons and Voss,
1998; Lim and Engstrom, 2001b; Bernard
and Fenton, 2002; Sampaio et al., 2003),
where 90–110 bat species are expected to
occur in sympatry (Voss and Emmons,
1996). Given the high diversity found in
other areas throughout Amazônia (Table 4,
Appendix) and the fact that estimated species richness of Jaú is already above 70 species even with low coverage and a conservative approach with a nonparametric estimator, we believe that with more sampling
effort and a better coverage, local species
richness of this area is likely to reach as
a minimum the expected number of species
estimated by Chao 1 (> 70), similarly to
other study sites in Amazônia (Table 4,
Appendix).
Within Jaú National Park, current sampling shows that number and composition
of sampled species vary both between and
within habitats. Part of this discrepancy is
linked to the fact that we only conducted
short-term surveys differing in capture
methodologies and capture effort. Bat species diversity within a habitat often appears
to be positively correlated with habitat complexity (Simmons and Voss, 1998; Bernard
TABLE 4. Jaccard similarity coefficient (J’) for bat faunas from nineteen localities in the Amazon basin arranged
in descendent order of similarity, compared with the bat fauna of Jaú. Number of localities follow the order
given in the text and on the map, see Fig. 1
Localities
# Shared species
4 Jaú
–
1 Jenaro Herrera
31
3 Serra do Divisor
28
6 Manaus
32
8 Xingú river
26
14 Iwokrama
38
9 Belém
25
12 Paracou
33
15 Kanunu mountains
34
16 Imataca
32
7 Alter do Chao
30
2 Cocha Cashu
27
11 Arataye
27
13 Sinnamary
21
18 Cunucunuma river
24
5 Ilha de Maracá
23
17 Canaima
32
10 Saül
23
19 and Serrania de los Pijiguaos and 20 Ticoporo
27
# Species
41
61
55
68
47
92
48
78
83
77
67
59
61
38
49
41
86
53
81
J’ Value (%)
–
44
42
42
42
40
39
38
38
38
38
37
36
36
36
36
34
32
28
Bats of Jaú National Park in Brazil
et al., 2001; Bernard and Fenton, 2002). As
white-sand habitats are neither structurally
complex nor highly stratified (see Pires and
Prance, 1985; Crome and Richards, 1988
and references therein), we would have
predicted low bat diversity in campina and
in campinarana. However, these habitats
had the highest local number of species of
all habitats that we sampled in Jaú. This is,
in our case, most likely a sampling bias,
caused by the fact that campina and campinarana were the only places where we
conducted echolocation recordings to document aerial insectivorous bats which are
usually missed or undersampled when only
mist-nets are used (Fenton and Bell, 1981;
Kalko, 1998; O’Farrell and Miller, 1999).
Further, due to the high structural complexity of terra firme, we expected high bat
species diversity in terra firme forests as has
been observed in bat assemblages elsewhere
in the Neotropics (see Reis and Peracchi, 1987; Brosset and Charles-Dominique,
1990; Brosset et al., 1996, 2001; Simmons
and Voss, 1998; Taddei and Pedro, 1998).
However, the known bat species number for
terra firme in Jaú is so far quite moderate
(n = 14 — Table 2). Given that the species
list of the entire park is only about 72%
complete (Chao 1), and that the sampling
period to date had been short, the lack of
concordance of habitat and species diversity clearly points towards the need for further long-term work within Jaú. When comparing habitats within Jaú, the current totals
for species numbers are more likely to reflect capture effort per habitat than any other causal factor. This is especially true for
the large areas of terra firme, the predominant habitat for the Park that has been comparatively little sampled to date.
Ecological Aspects
Our preliminary data also revealed some
interesting ecological aspects of the bat
113
species that are usually common in the region. As ecological information on most
neotropical bats is still scarce, we summarize these observations as follows:
(1) We captured three individuals of
Lonchophylla thomasi in the campinarana
sub-canopy. In the Reserva Duke, near Manaus, L. thomasi is very common along water courses in terra firme forests, where it is
the main pollinator of Caryocar glabrum
(Caryocaraceae) and Eperua duckeana
(Fabaceae: Caesalpinioideae — E. Fischer,
personal obs.). Both Caryocar and Eperua
are also common genera in the campinarana. In November 2000, we found a small
colony of three to five individuals in a fallen hollow log on the ground in a shaded
area with little ground cover in primary terra firme forest. The use of this type of roost
by L. thomasi was reported by Handley
(1976) in Venezuela and in Peru by Tuttle
(1970) and may be typical of the species.
(2) Although species of the genus
Carollia are very common in Neotropical
forests (e.g., Fleming et al., 1972; Brosset
and Charles-Dominique, 1990; Simmons
and Voss, 1998; Kalko and Handley, 2001;
Shapley et al., 2005), and represent the
most common species in areas near Manaus
(Sampaio et al., 2003, 2005), C. perspicillata was represented only by less than a third
(27.3%) of our samples (43 of 157 captures). Additionally, C. perspicillata was
not recorded in Campina.
(3) The absence of this genus from
campina and campinarana is probably
strongly related to dietary preferences and
the distribution of its food plants. Carollia
favors juicy, small-seeded infructescences,
mainly from pioneer plants such as Piper
spp. (Piperaceae) and Vismia spp. (Clusiaceae — Fleming and Heithaus, 1986;
Charles-Dominique, 1991; Ribeiro de Mello and Fernandez, 2000; Thies and Kalko,
2004). However, those do not constitute
dominant components of the campina flora
114
A. A. Barnett, E. M. Sampaio, E. K. V. Kalko, R. L. Shapley, E. Fischer, et al.
(see Pires and Prance, 1985). Fruits of Vismia sp. are also commonly eaten by C. perspicillata (Marinho-Filho and VasconcellosNeto, 1994) and were frequently found in
the faeces of individuals captured in igapó in 1998. Interestingly, this plant genus
occurs only rarely in igapó (Ribeiro et al.,
1999; Ferreira, 1997, 1999). However, it is
common in the transition zones between
igapó and terra firme (A. A. Oliveira, personal comm.). We conclude that C. perspicillata probably foraged there for Vismia
and commuted between different habitat
types.
(4) We also netted a small (n = 5) colony of Noctilio albiventris inhabiting a deep
pipe-like hole up the center of a living
Ocotea (Lauraceae) tree. The tree was situated on a mid-river sandbar that would have
been well under water in the rainy season.
A large mound of debris lay at the bottom of
the opening, the contents appeared to consist entirely of beetle elytra. Lacking sculpting and possessing a hydrodynamic shape,
the elytra studied were mostly from water
beetles including Hydrophilidae and Gyrinidae. No fish bones or remains from lepidopteran wings were found in the examined
faecal pellets. This supports observations
from Central America that N. albiventris is
mainly insectivorous, frequently eating
aquatic beetles (Fleming et al., 1972; Hood
and Pitoccheli, 1983; Kalko et al., 1998). Its
emergence pattern was very distinct. Both
the 1998 and 2000 surveys noted that the
activity peak for this species was within 15
minutes of sunset. Kalko et al. (1998) and
Fenton et al. (1993) recorded a similar pattern for this species.
(5) We compared our reproductive data
from Jaú with data from a study by Bernard (2002) conducted near Manaus ca. 220
km to the south-east. This author reported
reproductive peaks in January–February,
July, and October–November, coinciding
with local flowering and fruiting peaks.
A similar phenological periodicity occurs in
Jaú (Ferreira, 1997). Bernard (2002) recorded lactating Myotis riparius in October. In
Jaú, a lactating individual was caught in
early September, and a pregnant individual
was caught in July, suggesting agreement
with the pattern recorded in Manaus. In
contrast, a pregnant A. planirostris was
recorded in October in Jaú, while pregnant
and lactating females were netted in
Manaus only between March and August,
the local wet season. Species for which
there was concordance, such as A. cinereus,
C. perspicillata, and Tonatia bidens have
been recorded by Bernard (2002) as reproductively active in most months of the year.
Two other species, L. thomasi, and P. discolor had only single reproductive records at
both sites, respectively in November and
June in Jaú, and in October and July near
Manaus. In Jaú, a pregnant N. albiventris
was captured in November 2000. In the
1998 igapó survey, E. Bernard (personal
comm.) noted that during the same season
many captured male N. albiventris smelt
strongly and had pronounced scent glands,
suggesting reproductive activity. Furthermore, most adult females were lactating
when netted.
Species Distribution
In our preliminary inventory, we documented several rare species that were not
previously known from the area.
Originally collected in Santarém (Thomas, 1901), Saccopteryx gymnura is known
from only 13 specimens scattered between
several sites in Guyana, French Guiana, and
the lower Brazilian Amazon (see Lim and
Engstrom, 2001a, 2001b). Most individuals
have been captured in open areas, including
human-made clearings (Lim and Engstrom,
2001a, 2001b). This corresponds to the site
of the sound recordings that were made
in open, unobstructed habitats of campina
Bats of Jaú National Park in Brazil
and campinarana. However, the species’
acoustic identification given here is tentative and requires confirmation through
a voucher. If the presence of S. gymnura can
be confirmed, it represents a 600 km range
extension from Santarém.
Ametrida centurio, another bat that is
considered rare (Emmons and Feer, 1997),
was the second commonest bat at our site in
campina (7 out of 19 captures, 37%), a comparatively dry open habitat where the
canopy is rarely more than 3 m high. This
may indicate a preference of this species
for open areas, either above the canopy or
within the campina vegetation. This is not
completely in accordance with other studies (e.g., Brosset and Charles-Dominique,
1990; Rodríguez-Herrera and Hopkins,
2000; Bernard, 2001b; Kalko and Handley,
2001) that indicate that Ametrida centurio
prefers primary moist forests, where it flies
within rather than above the canopy.
Vampyriscus brocki is also known from
only few samples. It has recently been collected near Manaus (Bernard, 2002). We
mist-netted one individual at the edge of the
Seringalzinho village clearing. This was
not the first record for the country even
though Eisenberg and Redford (1999) state
that the species is not known from Brazil:
V. brocki has been already collected in the
states of Pará (Voss and Emmons, 1996) and
Rôndonia (USNM records: see Koopman,
1993; Simmons and Voss, 1998). Elsewhere
in the Amazon basin, V. brocki has been collected in south-eastern Peru by Ascorra et
al. (1996). Jaú is the fourth Brazilian site
from which this species is known. Members
of the genus appear to be specialized to
roost beneath palm fronds and the leaves of
larger herbaceous understory plants (see
Foster, 1992).
Molossops neglectus is known from less
than 30 specimens (Lim and Engstrom,
2001b). Its known distribution area is highly disjunct, with several potentially isolated
115
populations. It has been recorded from
north-eastern Argentina (Sekiama et al.,
2001), Peru (Depts. of Loreto and Pasco;
Ascorra et al., 1993), Colombia (Putumayo
state; Lim and Engstrom, 2001b), Venezuela (Bolívar state; Ochoa et al., 1993;
Ochoa, 1995) and Surinam (see Lim and
Engstrom, 2001b). A single Brazilian specimen has been collected near Belém, Pará
(Ascorra et al., 1991; Lim and Engstrom,
2001b). The echolocation recording from
Jaú is the first for the species in the entire
central Amazon basin and the fourth record
for Brazil — for other records see Sekiama
et al. (2001) in Paraná state and Pedro et al.
(2001) in Sno Paulo state. This represents
a range extension of over 1,000 km both
from Venezuela (Bolívar state) and from
the other closest Brazilian locality in Pará. Up until now, the species appeared to
have a circum-Amazonian distribution
(see Ascorra et al., 1991; Lim and Engstrom, 2001b; Sekiama et al., 2001). As
with S. gymnura, confirmation through
a voucher is needed to fully ascertain the
presence of this species.
The presence of Promops centralis was
also registered acoustically and confirmed
unambiguously by comparison with the
acoustic library of echolocation calls of aerial insectivorous bats of E. Kalko. Like
M. neglectus, this species was not previously known to occur in the Amazon basin (see
Koopman, 1993; Eisenberg and Redford,
1999). It is considered a rare but widespread
inhabitant of primary forest at the western
margins of Amazônia (e.g., basins of the
Napo and Ucayali river systems — see
Emmons and Feer, 1997). Recently, it was
reported for Acre (Nogueira et al., 1999)
and Pará states (Gregorin and Taddei,
2000), the latter confirming its occurrence
in eastern Brazil. It is also known from
a few records in Argentina (Massoia, 1980),
Paraguay (Myers and Wetzel, 1983), Bolivia (IbaZez and Ochoa, 1989; Anderson,
116
A. A. Barnett, E. M. Sampaio, E. K. V. Kalko, R. L. Shapley, E. Fischer, et al.
1991), Colombia (Marinkelle and Cadena,
1972), Ecuador (Reid et al., 2000), French
Guiana (Simmons and Voss, 1998), Guyana
(Lim and Engstrom, 2001b), Peru (Tuttle,
1970; Ascorra et al., 1993), and Surinam
(Genoways and Williams, 1979).
Comparing Results of Jaú with Other
Studies in Amazônia
The bat fauna of Jaú, as presented in this
paper, comprises about half (45%) of the
117 species listed by Marinho-Filho and Sazima (1998) for the Brazilian Amazon, and
38% of the 139 bat species known for Brazil
(Aguiar and Taddei, 1995). With a recorded
total of 53 species in 33 genera and 40 species determined by netting, the diversity of
the known bat fauna of Jaú is similar to other inventories when compared to other sampled areas in the area of the Amazon basin
(see Appendix). Those inventories, however, were based exclusively on mist-net
sampling and lacked acoustic data. We are
aware that inclusion of results of echolocation recordings would most likely lead to
much higher species numbers for these
localities. However, in terms of the relation of sampling effort to number and relative abundance of species recorded, Jaú exceeds values for other short-term inventories in lowland rainforest sites in the Brazilian Amazon and other Neotropical sites
(Table 5).
The total number of species recorded in
Jaú is notable given the comparatively short
time (about 44 days) over which the surveys
have been conducted. The results are similar to that of Robinson (1998) who worked
in Rorâima state and obtained 37 species
of bats during 56 days of fieldwork. Other examples of high-yield, short-term surveys include Pacheco et al. (1993), where
the authors reported over 50 co-existing
species of bats after several short-term surveys of a habitat-rich area in Manu, Peru.
Collecting sites ranged from tropical lowland forests to upper tropical forests and
moist grasslands. The high number of species in Jaú may be partly due to the temporal and spatial dispersion of the inventories.
Each was short but took place at a slightly
different time of year and in a different
habitat.
The nature of inventorial sampling
means that a high number of species is almost always caught in the first few days of
fieldwork (Simmons and Voss, 1998). Consequently, when the aim is to ascertain the
species composition of an area, short-term
inventories, although preliminary, provide
an effective sampling design in terms of
species-return per unit effort required to
record the 60–70% of the bat species
that we consider as a minimum for effective assessment of the conservation value of
a community. As nonparametric estimators
allow precise estimations of species richness only at species coverage of 60% or
more (Brose et al., 2003), inventories with
estimations of less than 60% are imprecise. Besides, the large number of habitat
TABLE 5. Comparison of mist-netting success in relation to capture effort at seven sites in Amazônia
Location (source)
Belém, Brazil (Kalko and Handley, 2001)
Manaus, Brazil (Bernard, 2001a)
Santarém, Brazil (Bernard et al., 2001)
Ilha de Maracá, Brazil (Robinson, 1998)
Potaro Plateau, Guyana (Shapley et al., 2005)
Acre, Brazil (Nogueira et al., 1999)
Jaú, Brazil (this study)
Sampling effort
1,955 mistnet-hours
2,375 mistnet-hours
2,019 mistnet-hours
≈ 530 mistnet-hours
57 nights
38 nights
1,001.5 net-hours
Number of
species
48
36
44
37
35
39
40
Number of
individuals
1,871
539
620
229
307
not stated
> 149
Bats of Jaú National Park in Brazil
types present in the park is very likely to
be another important contributory factor
to the bat species diversity of the region.
The 73 species that represent the potential
maximum of bat diversity in Jaú is closer
to the species numbers already known or
expected from other, well-sampled areas
in central Amazônia (see Appendix).
Bernard (2001b) reported 51 species from
primary forests around Manaus, for which
Chao 1 indicated a maximum of 58 species potentially occurring in the area.
Samples from the area around Manaus that
combined data from canopy mist-nets with
an extensive ground level inventory reached 72 species at an expected number of
70 based on Chao 1 (Sampaio et al., 2003).
In this case, Chao 1 underestimated species
richness.
Another example that is well suited to
show the effects of sampling effort with regard to time and methods on species coverage is the long-term survey in Paracou,
French Guiana, conducted by Simmons and
Voss (1998). Sampling included ground and
canopy mist-nets, as well as searches for
roosts. It resulted in more than 3,000 individuals and 78 species sampled within 168
nights. The degree of completeness reached
91% with Chao 1, with an expected richness
of 86 species. The expected value is higher
than the expected species richness for Jaú.
It is, however, close to the values already
reached in Iwokrama forest in the Guiana
region, obtained with a combination of
ground and canopy mist-nets.
The Iwokrama forest, Guyana, is with
92 species the locality with the highest
number of species recorded globally for any
tropical bat assemblage (Lim and Engstrom,
2001a, 2001b). This area is characterized by
high habitat heterogeneity that leads to altitudinally stratified vegetation types and thus
to a much higher regional habitat diversity
than found in the tropical lowland forests of
the Amazon basin.
117
Comparing the composition of bat
assemblages from central and eastern Amazônia, Bernard et al. (2001) found that the
level of faunal similarity of bat assemblages
decreased the further east the samples were
taken. This result is consistent with the conclusions reached by studies of terrestrial
non-volant mammals (e.g., Voss and Emmons, 1996), birds (Borges and Carvalhaes,
2000), and plants (Rizzini, 1963). In our
study, similary to the previous one, the Jaccard similarity coefficient suggests that the
bat fauna of Jaú tends to have its closest
affinities with sites in western Amazônia
and progressively lower similarity with geographically distant sites eastwards along
the Amazon river, and northwards towards
higher longitudes (Fig. 3 and Table 4).
We are aware that comparison of similarity is influenced by a range of factors, in
particular by the completeness of the respective samples. When compared to other,
long-term inventories, the Jaú bat fauna still
misses many species that have already been
reported for other Amazonian sites including Iwokrama, Paracou, Imataca, and
Cainama. This leads to lower similarity values than comparison of areas with comparable lower species numbers (see Table 4).
In general, the comparison of faunal similarity between different areas did not show
a clear trend that would indicate distinct
causal relationships. This may be: a) because the calculation of the Jaccard similarity coefficient uses only presence/absence
data of species and ignores proportionality of various species in a community;
b) because, as an index of similarity,
Jaccard does not include effects of species turnover rates, where some speciesrich genera (e.g., Artibeus, Micronycteris)
include species with more restricted distributions, while others, less species-rich
genera have wider distributions and their
representation changes little over wide
areas (e.g., Cormura, Rhynchonycteris,
118
A. A. Barnett, E. M. Sampaio, E. K. V. Kalko, R. L. Shapley, E. Fischer, et al.
Macrophyllum, Noctilio, Uroderma), and,
as mentioned above; c) because the sites
used for comparison, including Jaú, have
not yet been sampled well enough to make
such comparisons reliable.
Voss et al. (2001) compared the faunal
similarity of bats and non-volant mammals
in Amazônia, and showed that although the
similarity within the samples of bats and
non-volant mammals decreases with increasing distance, that this tendency is
weaker for bats (-8% per 1,000 km) than for
non-volant mammals (-14% per 1,000 km).
The authors also call attention to the higher
number of non-volant mammals that are endemic to the Amazon region than bats. Bats
are probably less limited by barriers such as
the Amazon river than non-volant species.
They also show variable degrees of specialisation and environmental requirements
(see similarity coefficient between Jaú
and Xingú, located at the southern margin
of Amazon river — Table 4). Bats also tend
to show relatively broad distributions (for
distribution maps see Emmons and Feer,
1997).
Comparing Results of Mist-netting and
Acoustic Surveys
We found that in Jaú about 80% of the
individuals netted (n = 197 individuals) and
64% of the species netted (n = 25 species)
were phyllostomid bats, while 83% of the
species registered acoustically (n = 18 species) were non-phyllostomid species. Nets
and bat detectors sample different bat guilds
(Kalko, 1998). Most phyllostomid bats emit
rather uniform, mostly weak, short and
steep frequency-modulated (FM), multiharmonic echolocation calls, whose main
energy is distributed across two to three harmonics (Thies et al., 1998; Kalko, 2004).
Furthermore, most signals are high-frequency. These call characteristics make most
phyllostomid bats difficult candidates for
acoustic surveys. However, phyllostomid
bats can be caught comparatively easily
with mist-nets, especially when these are set
in their flyways. In contrast, aerial insectivores (Emballonuridae, Molossidae, Mormoopidae, and Vespertilionidae) generally
produce louder calls at lower frequencies
with the main energy focused in the first or
second harmonic. Although aerial insectivorous bats tend to avoid nets, their call characteristics allow them to be more readily
identified with bat detectors than phyllostomids (e.g., Kalko and Schnitzler, 1998; Corben and O’Farrell, 1999; Miller and O’Farrell, 1999). Bats that were mainly documented through acoustic monitoring were
mostly composed of aerial insectivores
comprising the families Emballonuridae,
Mormoopidae, Molossidae, and Vespertilionidae. This part of the bat fauna is mostly missed or strongly underrepresented in
inventories as aerial insectivores cannot be
sampled well with mist-netting (Fenton and
Bell, 1981; Kalko, 1998; O’Farrell and Miller, 1999). Thus many of those species are
regarded as rare although they might be actually common in the area. The combined
results of the five Jaú surveys demonstrate
the usefulness of using both netting and
acoustic surveys in parallel during inventory work, even though the number of sound
recordings cannot be taken as equalling the
number of individuals. This complicates the
calculation of some standard measures of
diversity and similarity, such as the Simpson similarity coefficient. For indices that
take into account the relative abundances of
species, data from both methodologies cannot be combined in the same way. However,
similarity can be calculated separately for
aerial insectivores, assessed by acoustic
monitoring. The advantage to detect and
identify part of the bat fauna that is normally largely unexplored outweighs the disadvantage of comparability in terms of diversity indices.
Bats of Jaú National Park in Brazil
Conservation Considerations
The part of the bat fauna that was
sampled with mist-nets in Jaú was clearly
dominated by phyllostomid bats of the subfamilies Phyllostominae and Stenoderminae
(31% of the genera, 41% of all identified
species). Bats of these subfamilies reveal
highest species diversity in undisturbed
areas (Fenton et al., 1992; Brosset et al.,
1996). In Jaú we captured some rare species
(e.g., Lophostoma carrikeri, Macrophyllum
macrophyllum, Chrotopterus auritus — see
Brosset et al., 1996), and species most frequently known from undisturbed habitats
(e.g., Tonatia saurophila, Trachops cirrhosus — see Brosset et al., 1996; Bernard and
Fenton, 2002). We take this as a good indication of the near-pristine nature of Jaú’s
habitats.
The known chiropterofauna of Jaú includes a number of species that are rare
in local inventories, in particular A. centurio, V. brocki, Centronycteris maximilliani,
S. gymnura, M. neglectus and P. centralis.
Additionally, L. carrikeri has been reported
in Jaú by Gribel and Taddei (1989). Two
species in Jaú, A. centurio and S. gymnura,
are among the 13 species identified by
Marinho-Filho and Sazima (1998) as species occurring exclusively in the Amazon
region. In addition, L. carrikeri and S. gymnura are considered ‘vulnerable’ by the
IUCN (2003). Artibeus concolor, A. obscurus, Phyllostomus latifolius, and V. brocki
are classified as ‘near-threatened’ (Hutson,
2001; IUCN, 2003). Three more species
(Rhynchonycteris naso, Noctilio leporinus,
and C. auritus) are considered as ‘potentially vulnerable’ by Wilson (1996) because of
their rarity, specificity in roosting or dietary
specialization. Therefore, Jaú, like the
whole of Amazônia, includes species that
might be highly vulnerable, due to the low
number of known populations or individuals or specific habitat requirements (e.g.,
L. carrikeri, C. auritus). Since an effective
119
plan to protect large, still relative undisturbed patches of Amazonian forest, although ideal, is complex, long-term, and involves international and political approaches, the alternative has been mostly to study
and preserve local areas, which are at least
known to include ‘risk populations’. Jaú is
an example of such a site, which should be,
together with other Amazonian reserves,
considered important for the preservation of
a significant portion of the Amazonian bat
fauna.
Together, the five short surveys presented here represent the first preliminary picture of Jaú’s bat diversity. Because of the
potential importance of Jaú for the maintenance of biological diversity in Central
Amazônia in general and of bat diversity in
particular, we urge the undertaking of future
long-term bat inventory initiatives in the region. These must include a combination of
remote and hands-on recording methods to
obtain a more accurate idea of the bat fauna
of one of the most poorly known regions of
the Amazon basin. Establishment of more
long-term projects, including surveys
throughout the year, would greatly contribute to our knowledge of many of the region’s lesser-known species. Also, in Jaú,
plans for specific bat species could be taken
into consideration, where local populations
of at-risk species could be identified and
their protection prioritised. With our preliminary inventory we mean to call attention to
a site in Amazônia with a highly diverse bat
fauna. More research is needed to generate
local and national action plans to preserve
this high diversity also in the future.
ACKNOWLEDGEMENTS
We collectively thank FVA (particularly Muriel
Sarragossi, Sérgio Borges, José Luís Camargo, Marcos Pinheiro, Fernando Oliveira, Osmar and Maria da
Conceiçno Oliveira), IBAMA, Maria Nazareth F. da
Silva (curator of mammals at INPA, Manaus, Brazil),
and the late Charles O. Handley, Jr. (former curator of
120
A. A. Barnett, E. M. Sampaio, E. K. V. Kalko, R. L. Shapley, E. Fischer, et al.
mammals at the National Museum of Natural History,
Smithsonian Institution, Washington D.C., USA).
Rebecca Shapley and Adrian Barnett thank Bruce
Miller, Mark Engstrom, Mike O’Farrell, Eduardo and
Maria Elizio de Souza, Carolina Volkmar de Castilho,
Dalva, and Jacó. Funding for their fieldwork was provided by Bat Conservation International and Akodon
Ecological Consulting. Erica Sampaio and Elisabeth
Kalko thank Hans-Ulrich Schnitzler (University of
Tübingen, Germany) for continuous support. Funding
for Erica Sampaio was provided by the BDFFP (Biological Dynamics of Forest Fragmentation Project,
Manaus), WWF (World Wildlife Foundation) do Brasil, and by the Handley and Kalko Biodiversity Project (Smithsonian Institution). Erich Fischer especially thanks Juan Gabriel for field assistance; he also
thanks Ademir Costa de Oliveira, Alberto Vicentini,
Cosmo Fernandez, Jonas Ferreira Paz, Marcelo Gordo, Mike Hopkins, Selvino Neckel, Sérgio Borges for
help during field work, and Andrew Murchie for Jaú
images and vegetation maps. Funding for Erich Fischer and G. Camargo was provided by FVA and
CNPq. Enrico Bernard generously made available his
unpublished data from Jaú and commented on earlier
drafts of this paper. We thank Alexandre A. Oliveira
for identifying the Vismia seeds. This paper is dedicated to the memory of Charles O. Handley, Jr., a remarkable zoologist and bat researcher, as well as one
of our advisors, who passed away in 2000.
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Received 13 July 2005, accepted 17 February 2006
APPENDIX
Species matrix of 19 bat inventories for the Amazon rainforest used for comparison of fauna similarity
(Jaccard similarity coefficient), including Jaú. 1 — species sampled; 0 — species not sampled. Localities: Peru:
1 — Jenaro Herrera, 2 — Cocha Cashu; Brasil: 3 — Serra do Divisor, 4 — Jaú, 5 — Ilha de Maracá, 6 —
BDFFP, 7 — Alter do Chao, 8 — Río Xingú, 9 — Belém; French Guiana: 10 — Saül, 11 — Arataye, 12 —
Paracou, 13 — Sinnamary; Guyana: 14 — Iwokrama forest, 15 — Kanunu mountains; Venezuela: 16 —
Imataca, 17 — Canaima, 18 — Río Cunucunuma, 19 — Ticoporo and La Serrania de los Pijiguaos
Species
Centronycteris maximiliani
Cormura brevirostris
Diclidurus albus
D. ingens
D. isabellus
D. scutatus
Peropteryx klappleri
P. leucoptera
P. macrotis
Rhynchonycteris naso
Saccopteryx bilineata
S. canescens
S. gymnura
S. leptura
Desmodus rotundus
Diaemus youngi
Diphylla ecaudata
Anoura caudifera
A. geoffroyi
A. latidens
Glossophaga commissarisi
G. longirostris
G. soricina
Lionycteris spurrelli
Choeroniscus minor
C. godmani
Lonchophylla mordax
L. thomasi
Lichonycteris obscura
Scleronycteris ega
1
0
0
0
0
0
0
1
1
0
1
1
0
0
1
1
0
0
1
0
0
0
0
1
0
1
0
1
1
0
0
2
0
0
0
0
0
0
0
0
0
1
1
0
0
1
1
0
1
1
0
0
1
0
1
0
1
0
0
1
0
0
3
0
0
0
0
0
0
0
0
0
1
1
0
0
1
1
1
1
1
0
0
0
0
1
0
1
0
0
1
0
0
4
1
1
0
0
0
0
0
0
0
1
1
1
0
1
1
1
0
0
0
0
0
0
1
0
0
0
0
1
0
0
5
0
1
0
0
0
0
0
0
0
1
1
1
0
1
1
0
0
0
0
0
0
0
1
0
1
0
0
1
0
0
6
1
1
0
0
0
0
0
1
0
0
1
1
0
1
1
1
0
1
0
0
0
0
1
1
1
0
0
1
1
0
7
0
0
0
1
0
0
0
0
1
1
1
1
0
0
1
0
0
0
0
0
0
0
1
0
1
0
0
1
1
1
8
0
0
0
0
0
0
0
0
1
1
1
1
0
1
1
0
1
1
0
0
0
0
1
0
1
0
0
1
0
0
9 10 11 12 13 14 15 16 17 18 19
0 0 0 1 0 1 0 0 0 0 0
1 1 1 1 0 1 1 1 0 1 1
0 0 0 0 0 1 0 1 0 0 0
0 0 0 0 0 1 0 0 0 0 0
0 0 0 0 0 1 0 0 0 0 0
0 0 1 1 0 0 1 1 0 0 0
0 0 0 1 0 0 0 1 0 0 0
0 0 0 1 0 1 0 0 0 0 0
1 0 1 1 0 1 1 1 0 1 1
1 0 0 1 1 1 1 1 1 1 1
1 1 1 1 1 1 1 1 1 1 1
1 0 0 0 0 1 1 1 1 0 1
1 0 0 1 0 1 0 0 0 0 0
1 1 1 1 0 1 1 1 1 1 0
1 1 1 1 1 1 1 1 1 1 1
1 0 0 1 0 1 1 0 1 0 0
0 0 0 0 0 0 0 0 0 0 0
0 1 1 1 0 0 1 0 1 1 0
0 0 1 0 0 1 0 1 1 0 1
0 0 0 0 0 1 0 1 1 0 0
0 0 0 0 0 0 0 0 0 0 0
0 0 0 0 0 0 1 0 1 0 1
1 1 1 1 1 1 1 1 1 1 1
1 1 1 0 0 1 1 1 1 1 1
1 1 1 1 0 1 0 1 1 0 0
0 0 0 0 0 0 1 0 0 0 0
0 0 0 0 0 0 0 0 0 0 0
1 1 1 1 1 1 1 1 1 0 1
1 0 0 1 0 1 0 1 1 0 0
0 0 0 0 0 0 0 0 0 1 0
126
A. A. Barnett, E. M. Sampaio, E. K. V. Kalko, R. L. Shapley, E. Fischer, et al.
APPENDIX. Continued
Species
Chrotopterus auritus
Glyphonycteris daviesi
G. sylvestris
Lampronycteris brachyotis
Lonchorhina aurita
L. orinocensis
L. inusitata
Lonchorhina sp.
Lophostoma brasiliense
L. carrikeri
L. schulzi
L. silvicolum
Macrophyllum macrophyllum
Micronycteris brosseti
M. hirsuta
M. homezi
M. megalotis
M. microtis
M. minuta
M. schmidtorum
Mimon bennettii
M. crenulatum
Phylloderma stenops
Phyllostomus discolor
P. elongatus
P. hastatus
P. latifolius
Tonatia saurophila
Trachops cirrhosus
Trinycteris nicefori
Vampyrum spectrum
Carollia brevicauda
C. castanea
C. perspicillata
Rhinophylla fischerae
R. pumilio
Sturnira lilium
S. magna
S. tildae
Ametrida centurio
Artibeus amplus
A. anderseni
A. cinereus
A. concolor
A. glaucus
A. gnomus
A. lituratus
A. obscurus
A. planirostris
Chiroderma trinitatum
C. villosum
Enchisthenes hartii
1
1
0
0
0
0
0
0
0
1
1
0
1
0
0
0
0
1
0
0
0
0
1
1
1
1
1
0
1
1
1
1
1
1
1
1
1
1
0
1
0
0
1
0
1
0
1
1
1
1
1
1
1
2
1
0
0
0
0
0
0
0
1
0
0
1
1
0
0
0
1
0
1
1
0
1
1
0
1
1
0
1
1
0
1
1
1
1
0
1
1
0
1
0
0
1
1
0
1
1
1
1
1
1
1
0
3
1
0
0
0
0
0
0
0
0
0
0
1
1
0
1
0
1
0
1
0
0
0
0
1
1
1
0
1
1
1
1
1
1
1
1
1
1
1
1
0
0
1
1
0
0
0
1
1
0
1
1
0
4
1
0
0
0
0
0
0
0
0
1
0
0
1
0
0
0
0
0
0
0
0
0
0
0
1
1
1
1
1
0
0
1
0
1
0
1
0
0
1
1
0
1
1
1
0
0
1
1
1
0
0
0
5
0
0
1
0
1
0
0
0
1
0
0
0
0
0
1
0
1
0
1
0
0
1
1
1
1
1
0
1
0
1
0
0
0
1
0
1
1
0
1
0
0
1
0
1
0
0
1
1
1
0
1
0
6
1
1
1
1
0
0
0
0
1
1
1
1
0
0
1
0
1
1
1
1
0
1
1
1
1
1
1
1
1
1
1
1
0
1
0
1
1
0
1
1
0
0
1
1
0
1
1
1
1
1
1
0
7
1
1
1
1
0
0
0
0
1
1
0
1
0
0
1
1
1
0
1
1
0
1
1
1
1
1
0
1
1
1
1
1
0
1
1
1
1
0
1
1
0
1
1
1
0
1
1
1
1
1
1
0
8
1
1
1
0
0
0
0
0
1
0
0
1
1
0
0
0
1
0
0
0
0
0
0
1
1
1
0
1
1
1
0
0
0
1
1
1
1
0
1
0
0
0
1
1
0
1
1
1
1
0
1
0
9 10 11 12 13 14 15 16 17 18 19
1 1 1 1 0 1 1 1 1 1 1
1 0 0 1 0 1 0 1 1 0 1
0 1 1 1 1 1 1 0 1 0 1
0 0 0 0 0 1 0 0 1 0 0
0 0 0 0 0 1 0 0 1 0 0
0 0 0 0 0 0 0 0 0 0 1
0 1 0 0 0 0 0 0 0 0 0
0 1 1 0 0 0 0 0 0 1 0
1 1 0 1 1 1 1 1 1 0 1
1 0 0 1 1 1 0 0 1 0 1
0 1 1 1 1 1 0 0 0 0 0
1 1 1 1 1 1 1 1 1 1 1
0 0 1 1 1 1 1 1 1 1 0
0 1 0 1 0 1 0 0 0 0 0
0 1 0 1 1 1 0 0 1 0 1
0 0 0 1 0 1 0 0 0 0 0
0 1 1 1 1 1 1 1 1 1 1
0 0 0 1 0 1 0 1 1 1 0
1 0 0 1 1 1 1 1 1 0 0
0 0 0 1 0 0 0 0 1 1 0
0 1 1 1 0 0 0 0 0 0 0
1 1 1 1 1 1 1 1 1 0 1
0 1 1 1 1 1 1 1 1 1 1
0 0 1 1 0 1 1 1 1 0 1
1 1 1 1 0 1 1 1 1 1 1
1 1 1 1 0 1 1 1 1 1 1
0 1 1 0 0 0 1 0 0 0 0
1 1 1 1 0 1 1 1 1 0 1
1 1 1 1 1 1 1 1 1 0 1
1 1 1 1 1 1 1 1 1 0 1
1 1 1 1 0 1 0 1 1 0 1
1 1 1 0 1 1 1 1 1 1 1
0 0 0 0 0 0 0 0 1 0 0
1 1 1 1 1 1 1 1 1 1 1
0 0 0 0 0 0 0 0 0 0 0
1 1 1 1 1 1 1 1 1 1 0
1 1 1 1 1 1 1 1 1 1 1
0 0 0 0 0 0 0 0 0 0 0
1 1 1 1 1 1 1 1 1 1 0
1 1 1 1 0 1 1 1 1 1 1
0 0 0 0 0 0 1 0 1 1 1
0 0 0 0 0 0 0 0 0 0 0
1 1 0 1 1 1 1 1 1 0 1
0 0 1 1 0 1 1 1 1 1 0
0 0 0 0 0 1 1 1 1 1 0
1 1 1 1 1 1 1 1 1 1 0
1 1 1 1 1 1 1 1 1 1 1
1 1 1 1 1 1 1 1 1 1 1
1 1 1 1 1 1 1 1 1 1 1
1 0 1 1 0 1 0 1 1 1 1
1 0 1 1 0 1 1 1 1 1 1
0 0 0 0 0 0 0 0 1 0 0
Bats of Jaú National Park in Brazil
127
APPENDIX. Continued
Species
Mesophylla macconnelli
Platyrrhinus aurarius
P. brachycephalus
P. helleri
P. infuscus
P. lineatus
Sphaeronycteris toxophyllum
Uroderma bilobatum
U. magnirostrum
Vampyriscus bidens
V. brocki
Vampyressa melissa
V. thyone
Vampyrodes caraccioli
Pteronotus davyi
P. gymnonotus
P. parnellii
P. personatus
Mormoops megalophylla
Noctilio albiventris
N. leporinus
Furipterus horrens
Thyroptera discifera
T. lavali
T. tricolor
Natalus tumidirostris
Cynomops abrasus
C. greenhalli
C. paranus
C. planirostris
Eumops auripendulus
E. bonariensis
E. glaucinus
E. hansae
E. maurus
E. perotis
E. trumbulli
Molossops mattogrossensis
M. neglectus
M. temminckii
Molossus aztecus
M. barnesi
M. coibensis
M. currentium
M. molossus
M. rufus
M. sinaloae
Nyctinomps gracilis
N. laticaudatus
N. macrotis
Promops centralis
P. nasutus
1
1
0
1
1
0
0
0
1
1
0
1
0
1
0
0
0
0
0
0
1
0
1
1
0
1
0
0
0
0
0
0
0
0
0
0
0
0
0
1
0
0
0
0
0
1
1
0
0
0
0
1
0
2
0
0
1
1
1
0
1
1
1
1
0
0
1
1
0
0
0
0
0
1
1
1
0
0
1
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
1
0
0
0
1
0
0
0
3
1
0
1
1
1
0
0
1
1
1
0
0
1
1
0
0
0
0
0
1
1
0
0
0
1
0
0
0
0
0
1
0
0
0
0
0
0
0
0
0
0
0
0
0
1
0
0
0
0
0
1
0
4
1
0
0
0
0
0
0
0
0
0
1
0
0
0
0
0
0
0
0
1
1
0
0
0
0
0
0
0
0
0
0
1
0
0
0
0
0
0
1
0
0
0
0
0
1
0
0
0
0
0
1
0
5
1
0
0
0
0
0
0
1
0
0
0
0
0
0
0
1
1
1
0
0
1
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
1
0
0
0
1
0
0
0
6
1
0
0
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
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
1
1
0
0
0
0
0
0
0
7
1
0
1
1
0
0
0
1
1
1
0
0
0
0
0
1
1
0
0
1
0
0
0
0
1
0
0
0
1
1
0
1
0
0
0
0
0
0
0
0
0
0
0
0
1
0
0
0
0
0
0
0
8
1
0
0
1
0
0
0
1
1
0
1
0
0
0
0
0
1
0
0
1
0
1
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
1
0
0
0
0
0
0
0
0
0
0
0
0
0
0
9 10 11 12 13 14 15 16 17 18 19
1 0 1 1 1 1 1 1 1 0 0
0 0 0 0 0 0 0 0 1 0 1
0 0 0 0 1 0 0 1 1 0 0
1 1 1 1 1 1 1 1 1 1 1
0 0 0 0 0 0 0 0 0 0 0
0 0 1 0 0 0 0 0 0 0 0
0 0 0 0 0 0 0 0 1 0 1
1 1 1 1 1 1 1 1 1 1 1
1 0 0 0 0 0 1 1 1 0 1
1 0 1 0 0 1 1 1 1 1 1
0 0 1 1 0 1 0 0 0 0 0
0 0 1 0 0 0 0 0 0 0 0
0 0 1 0 0 1 0 1 1 0 1
1 1 0 0 1 1 0 1 1 1 1
0 0 0 0 0 0 0 0 1 0 1
0 0 0 0 0 1 1 0 1 0 0
0 1 1 1 0 1 1 1 1 1 1
0 0 0 0 0 1 0 0 1 0 1
0 0 0 0 0 0 0 0 1 0 0
0 0 0 1 1 1 1 1 1 0 0
0 0 0 1 1 1 1 1 1 1 1
0 1 0 1 0 0 1 0 1 1 0
0 0 0 0 0 0 1 0 0 0 0
0 0 0 0 0 0 0 0 0 0 0
0 1 1 1 0 1 1 1 1 1 0
0 0 0 0 0 0 1 0 1 0 1
0 0 0 1 0 1 0 1 0 0 1
0 0 1 0 0 0 0 1 0 0 1
0 0 0 1 0 1 1 1 0 0 1
0 1 1 0 0 0 1 0 0 0 1
0 1 0 1 0 1 1 1 0 0 1
0 0 0 0 0 0 1 0 0 0 0
0 0 0 0 0 0 1 0 0 0 1
0 1 1 1 0 1 1 1 0 0 1
0 0 0 0 0 0 1 0 0 0 1
0 0 0 0 0 0 1 0 0 0 1
0 0 0 0 0 0 1 0 0 0 1
0 0 0 0 0 0 1 0 0 0 1
0 0 0 0 0 1 0 1 0 0 1
0 0 0 0 0 0 1 0 0 0 1
0 0 0 0 0 0 0 0 0 0 1
0 0 0 1 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 0 0 0 0
0 1 1 1 1 1 1 1 0 1 1
0 0 1 1 0 1 1 1 0 1 1
0 0 0 1 0 1 0 0 0 0 0
0 0 0 0 0 0 0 0 0 0 1
0 0 1 0 0 0 1 1 0 1 1
0 0 0 0 0 1 1 0 0 0 1
0 0 0 1 0 1 0 0 0 0 1
0 0 0 0 0 0 1 0 0 0 1
128
A. A. Barnett, E. M. Sampaio, E. K. V. Kalko, R. L. Shapley, E. Fischer, et al.
APPENDIX. Continued
Species
Eptesicus andinus
E. brasiliensis
E. chiriquinus
E. furinalis
Lasiurus atratus
L. blossevillii
L. castaneus
L. cinereus
L. ega
L. egregius
Rhogeessa io
Myotis albescens
M. keaysi
M. nigricans
M. oxyotus
M. riparius
M. simus
Total number of species
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19
0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 1 0 0
1 0 0 1 0 0 1 0 0 0 0 0 0 1 1 1 1 1 1
0 0 0 0 0 1 1 0 1 0 0 1 0 1 0 1 0 0 0
0 0 0 0 0 0 0 0 0 1 0 1 1 0 1 1 1 0 0
0 0 0 0 0 0 0 0 0 1 0 0 0 1 0 1 0 0 0
0 0 0 0 0 0 1 0 0 0 0 1 0 1 1 0 1 0 0
0 0 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0
0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1
0 1 1 0 0 0 0 0 0 0 0 0 0 0 1 0 1 0 1
0 0 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0 0
0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 1 0 1
1 1 1 1 0 1 1 1 0 0 0 0 0 1 1 0 1 1 0
0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1
1 1 0 1 1 1 0 0 0 0 1 1 1 1 1 1 1 1 1
0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 0
1 1 1 1 0 1 1 1 0 1 1 1 0 1 0 1 1 0 1
1 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
61 59 55 41 41 68 67 47 48 53 61 78 38 92 83 77 86 49 81