Morcegos e áreas restauradas: uma via
de mão dupla
Ariovaldo P. Cruz-Neto
Departamento de Zoologia, IB, UNESP, Rio Claro, SP
Simpósio: Morcegos como pilares da natureza
Simpósio:
Morcegos como pilares da natureza
Morcegos e Áreas Restauradas: Uma Via de Mão Dupla
Ariovaldo P. Cruz-Neto
Departamento de Zoologia, IB, UNESP, Rio Claro, SP
Restauração Florestal Iniciar (ou acelerar) recuperação de ecossistemas
(integridade e sustentabilidade)
Restaurar forma, função e processos
ecossistêmicos a níveis pré-distúrbio
Restauração Florestal Morcegos Frugívoros Métricas de Efetividade
Recuperação da
biodiversidade
Recrutamento de espécies
alóctones
Anemocórica
Zoocórica
Banco de sementes
Chuva de sementes
Qual a importância dos morcegos
frugívoros para o sucesso de
projetos de restauração?
Contribuição significativa para o
aporte de sementes alóctones
Acta Oecologica 37 (2011) 31e36
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journal homepage: www.elsevier.com/locate/actoec
Original article
Author's personal copy
Frugivory by phyllostomid bats (Mammalia: Chiroptera) in a restored
area in Southeast Brazil
b
Acta Oecologica
37 (2011)
31e36 Port-Carvalho c, Simone Godoi d,
Maurício Silveira a,1, Leonardo
Trevelin
, Marcio
Elizabeth Neuenhaus Mandetta a, Ariovaldo P. Cruz-Neto b, *
a
Departamento de Botânica, Universidade
Estadual
(UNESP),at
Av.ScienceDirect
24-A, 1515, 13506-900 Rio Claro, São Paulo, Brazil
Contents
listsPaulista
available
Departamento de Zoologia, Universidade Estadual Paulista (UNESP), Av. 24-A, 1515, 13506-900 Rio Claro, São Paulo, Brazil
c
Divisão de Florestas e Estações Experimentais, Instituto Florestal, Av. Rodrigues Alves 38-25, 17013-000 Bauru, São Paulo, Brazil
d
Departamento de Botânica, Universidade de São Paulo (USP), Rua do Matão 277, Caixa Postal 1461, 05422-970 São Paulo, SP, Brazil
b
Acta Oecologica
a r t i c l e i n f o
a b s t r a c t
journal homepage: www.elsevier.com/locate/actoec
Article history:
Received 26 January 2010
Accepted 10 November 2010
Available online 13 December 2010
article
We studied the potential contribution of frugivorous bats to the reestablishment of vegetational diversity
in a restored area. We analysed the diets of the bat species and the differences between them in the
consumption of fruits of autochtonous and allochthonous species. Planted (autochtonous) species were
the basis of diets, especially Solanum mauritianum and Cecropia pachystachya, whereas for allochthonous
species we found that Piperaceae to be of particular importance. Carollia perspicillata was the main seed
disperser for allochthonous species, and potentially the most important bat in the promotion of vegetation diversity in the study area. Our results suggest that frugivorous bats are especially important in the
reestablishment of vegetation in disturbed areas, and that restorarion efforts should focus on the
planting of different zoochorous species that would guarantee a high year-round fruit production,
thereby facilitating natural
c plant reestablishment bydfrugivorous bats in regenerating areas.
! 2010 Elsevier Masson SAS. All rights reserved.
2011
Keywords:
vory by phyllostomid
bats (Mammalia: Chiroptera) in a restored
Seed dispersal
Diet
n Southeast
Brazil
Frugivorous bats
a, 1
Ecological restoration
Semi deciduous forests
io Silveira , Leonardo Trevelin b, Marcio Port-Carvalho , Simone Godoi ,
th Neuenhaus Mandetta a, Ariovaldo P. Cruz-Neto b, *
nto de Botânica, Universidade Estadual Paulista (UNESP), Av. 24-A, 1515, 13506-900 Rio Claro, São Paulo, Brazil
nto de Zoologia, Universidade Estadual Paulista (UNESP), Av. 24-A, 1515, 13506-900 Rio Claro, São Paulo, Brazil
1. Introduction
Rodrigues, 2002; Zamora and Montagnini, 2007). Seed rain
Florestas e Estações Experimentais, Instituto Florestal, Av. Rodrigues Alves 38-25, 17013-000 Bauru, São Paulo, Brazil
involves
either
nto de Botânica, Universidade de São Paulo (USP), Rua do Matão 277, Caixa Postal 1461, 05422-970 São
Paulo, SP,
Brazilthe recruitment of seeds from planted trees
Ecological restoration is an intentional activity that initiates or
(autochtonous seeds), or from colonist trees (i.e. allochthonous
dels for such studies. Within Neotropical bats assemblages,
ng species constitute the dominant and most diverse guild
of feeding habits (Kalko, 1998; Medellin et al., 2000;
eating phyllostomid bats to the input of allochthonous seeds in
a restored area in Southeast Brazil. We address two basic questions:
a) what are the diets of the fruit-eating bat species already resident
RPPN Parque São Marcelo
(International Paper – Mogi Guaçu, SP)
2002/2003 – Programa restauração # 2
•  240 ha – Resolução SMA 47/2003
•  101 espécies de plantas
Fig. 1. Localization and general characterization of the RPPN São Marcelo in São Paulo State, Brazil.
programs. The difference in the consumption of autochtonous and
allochthonous species by the fruit-eating bats were analysed by
a c2 test. The association between the variables “resource” and “bat
species” is indicative of the potential of different bat species to
disperse allochthonous seeds into the restored areas as well as an
indicative of the degree by which the bats depend on autochthonous plant species as food resources.
Table 1
Planted species reported to be consumed by bats in a restored area.
Plant species
Araliaceae
Dendropanax cuneatum Decne & Planch.
Cecropiaceae
Cecropia pachystachya Trec.
Fabaceae
Inga uruguensis Hooker et Arnot
Copaifera langsdorfii Desf.
Holocalyx balansae Mich.
Moraceae
Ficus citrifolia Schodat
Maclura tinctoria (L.) D. Don ex Steud.
Myrtaceae
Eugenia uniflora L.
Psidium guajava L.
Sapindaceae
Sapindus saponaria L.
Solanaceae
Solanum mauritianum Scop.
Sterculiaceae
Guazuma ulmifolia Lam.
34Identification of plant species was carried
Institute of Sao Paulo, Brazil.
Successional stage
2005/2006 Fruiting
Late successional
Pioneer
X
Pioneer
Late successional
Late successional
X
2.3. Fruit availability
We carried out a fruit availability survey between March 2005
and February 2006, aiming to track the availability of species
consumed by bats in the restored area. This data was used to
Pioneer
X
evaluate if individuals of the autochthonous species consumed by
Late successional
bats were producing fruits during the sampling periods. If they
were not, we assumed that bats to be consuming fruits from indiLate successional
X
viduals of these species located outside the restored area. Plant
Pioneer
X
species that did not produce fruits were not included in this study.
Late successional
Fruiting of chiropterocoric species planted in the area (Table 1) was
assessed monthly, and we registered presence or absence of ripe
Pioneer
X
fruits on each sampled individual. Number of marked individuals
Pioneer
X
for each species was based on its availability in sampled plots, and
varied from 33 individuals of Solanum mauritianum to one indiout by specialists from
Botanical
M. The
Silveira
et al. / Acta Oecologica 37 (2011) 31e36
vidual of Ficus citrifolia.
Author's personal copy
Table 2
List of fruit-eating phyllostomid bats captured within the restored area during the
study period. Numbers indicate the total number of individuals of each species
captured during the study and does not include recaptures.
Number of captures
(%)
Artibeus lituratus (Al)
Platyrrhinus lineatus (Pl)
Sturnira lilium (Sl)
Carollia perspicillata (Cp)
Glossophaga soricina (Gs)a
Vampyressa pusilla (Vp)
Pygoderma bilabiatum (Pb)
Phyllostomus discolor
258
81
80
77
24
5
3
1
48.8
15.3
15.1
14.6
4.5
0.9
0.6
0.2
Total
529
100
a
Although G. soricina has a diet mostly based on nectar and pollens, it was
included in this study as we found seeds remain in its feces.
Frequency of Occurence (%)
Species
100
Artibeus lituratus
100
80
80
60
60
40
40
20
20
0
0
100
80
60
Sturnira lilium
100
80
Carollia perspicillata
Plathyrrinus lineatus
Fotos: www.casadosmorcegos.org
60
Author's personal copy
M. Silveira et al. / Acta Oecologica 37 (2011) 31e36
2
fruit-eating phyllostomid bats captured within the restored area during the
period. Numbers indicate the total number of individuals of each species
ed during the study and does not include recaptures.
Number of captures
(%)
beus lituratus (Al)
yrrhinus lineatus (Pl)
nira lilium (Sl)
llia perspicillata (Cp)
sophaga soricina (Gs)a
pyressa pusilla (Vp)
oderma bilabiatum (Pb)
lostomus discolor
258
81
80
77
24
5
3
1
48.8
15.3
15.1
14.6
4.5
0.9
0.6
0.2
529
100
l
though G. soricina has a diet mostly based on nectar and pollens, it was
ed in this study as we found seeds remain in its feces.
esults
mauri+anum We mist-netted 542Solanum individuals
of eight species of predomiy or exclusively frugivores phyllostomid bats during our study,
the exception of Glossophaga soricina which also feeds on
ar and pollen, and Phyllostomus discolor, considered an
vorous species, both with records of frugivory in other regions
ig et al., 1993; Zortéa, 2003; Sato et al., 2008). The most
mon species were, in ranked order, Artibeus lituratus, Platyrs lineatus, Sturnira lilium and Carollia perspicillata (Table 2). We
ned a total of 184 fecal samples from a total of six species. Of
e, 182 contained plant materials, and two consisted entirely of
opods remains. The great majority of fecal samples contained
one type of seeds (91%) and the two most common bat species
Frequency of Occurence (%)
cies
100
100
Artibeus lituratus
80
80
60
60
40
40
20
20
0
0
100
100
Sturnira lilium
80
80
60
60
40
40
20
20
0
0
Cp
Fsp
Pa
Pu
Carollia perspicillata
Sm
NI
Plathyrrinus lineatus
Cp
Fsp
Pa
Pu
Sm
NI
Plant Species
Fig. 2. Frequency of occurrence (%) of different plant species in fecal samples of the bats
Artibeus lituratus, Carollia perspicillata, Sturnira lilium and Platyrrhinus lineatus. Cp e
Cecropia pachystachya. Fsp e Ficus spp. Pa e Piper aduncum. Pu e Photomorpha umbellata.
Sm e Solanum mauritianum. NI e Non-identified morphotype.
the
ae e
main
d C.
established in the restored area, but none presented fruit production
during this study. Even so, seeds from both species were encountered
Consumo
de plantas alóctones
in bats feces collected in various months, reaffirming the allochthoArtibeus
Carollia
87%
nous
nature ofethis
sample.– In
contrast, all autochtonous species
consumed by bats during our study produced fruit in the restored
d area
from
seeds
of bat
70
6% otal
37
9
5
15
3
11
2
82
ation
Number of Sampes
60
Piper aduncum
50
40
33% 30
20
10
0
Artibeus lituratus
Carollia perspicillata
Fig. 3. Number of fecal samples containing autochtonous (closed bars) and allochthonous (open bars) seeds for Artibeus lituratus and Carollia perspicillata.
Photomorpha umbellata
Restauração Florestal Morcegos Frugívoros Atração da fauna
Reestabelecimento de
padrões de história de vida
Áreas restauradas proporcionam aos
morcegos novos habitats de forrageio e
abrigo?
2008 •  5 sessões de 4 a 8 dias
•  Estação seca e chuvosa
A. lituratus (n = 10) C. perspicillata (n = 11) 1)  Área de vida e área de forrageio (Kernel 95% FE)
2)  Uso do Habitat (Compositional Analysis)
3)  Relação com fenologia dos recursos
(dentro da área restaurada)
4) Localização de abrigos
Author's personal copy
Forest Ecology and Management 291 (2013) 136–143
Contents lists available at SciVerse ScienceDirect
Forest Ecology and Management
journal homepage: www.elsevier.com/locate/foreco
Author's personal copy
Use of space by frugivorous bats (Chiroptera: Phyllostomidae) in a restored
Atlantic forest fragment in Brazil
a,⇑
Forest Ecology and Management 291 (2013) 136–143
b,1
Leonardo C. Trevelin , Maurício Silveira , Marcio Port-Carvalho c, Daniel H. Homem a,
Ariovaldo P. Cruz-Neto a Contents lists available at SciVerse ScienceDirect
a
Departmento de Zoologia, Universidade Estadual Paulista (UNESP), Av. 24-A, 1515, CEP 13506-900, Rio Claro, SP, Brazil
Departamento de Botânica, Universidade Estadual Paulista (UNESP), Av. 24-A, 1515, CEP 13506-900, Rio Claro, SP, Brazil
c
Divisão de Florestas e Estações Experimentais – Instituto Florestal, Av. Rodrigues Alves 38-25, CEP 17013-000, Bauru, São Paulo, Brazil
b
a r t i c l e
Forest Ecology and Management
i n f oj o u r n a l h o m e paabg e
s :twrwawc. e
t lsevier.com/locate/foreco
2013
Article history:
Received 6 April 2012
Received in revised form 7 November 2012
Accepted 9 November 2012
We studied patterns in the use of space for foraging and roosting by two frugivorous bat species in a fiveyear-old restored Atlantic forest located in a fragmented landscape in southeastern Brazil. Ten individuals
of Carollia perspicillata and eleven individuals of Artibeus lituratus were monitored through radio-telemetry
in five sampling sessions. Each session lasted 3–8 days for each individual, with an average of 25.4 ± 10
locations for each C. perspicillata individual and 19 ± 4.4 for each A. lituratus individual. We described an
average range of 124.4 ha and an average commuting distance of 1158.8 m for A. lituratus and an average
Keywords:
range and commuting distance of 32 ha and 489 m, respectively, for C. perspicillata. We demonstrated a
Artibeus
consistent pattern in habitat use and movements for both studied species, where they strictly used forests
Carollia
(restored or not) for day roosting, roosting in the foliage of trees located only in secondary forest remnants
Day roost
a,⇑
b,1
and restored areas, while restored areascwere their main feeding habitat.a We demonstrate that newly
Habitat use
restored forests can be readily incorporated as foraging and roosting habitats by these species, and that
Radio-telemetry
a
Range area
C. perspicillata alters its roosting behavior in relation to preferred food availability. These results, when
combined with data on the diet of the studied species, show consistent evidence of the potential that bats
Departmento de Zoologia, Universidade Estadual Paulista (UNESP), Av.have
24-A,
CEPspecies
13506-900,
Rio Claro,
SP, Brazil
to1515,
improve
diversity
of anthropogenic
plantings with their own natural seed dispersal.
Departamento de Botânica, Universidade Estadual Paulista (UNESP), Av. 24-A, 1515, CEP 13506-900, Rio Claro, SP, Brazil
! 2012 Elsevier B.V. All rights reserved.
Use of space by frugivorous bats (Chiroptera: Phyllostomidae) in a restored
Atlantic forest fragment in Brazil
eonardo C. Trevelin , Maurício Silveira
Ariovaldo P. Cruz-Neto
, Marcio Port-Carvalho , Daniel H. Homem ,
of feeding habits (Kalko, 1998; Medellin et al., 2000;
a) what are the diets of the fruit-eating bat species already resident
Arc Gis - georeferenciamento
e mapa digital
(2.855,23 ha))
Disponibilidade relativa de habitats
Maximum Sampling Circle (MSC)
43,87 % Área Antropizada
19,96 % Floresta Secundária
18,39% Floresta de Eucalipto
9,24% Área restaurada (2003)
8,53 % Área Restaurada (1996)
Fig. 1. Localization and general characterization of the RPPN São Marcelo in São Paulo State, Brazil.
marked individuals. Each individual was monitored for all four
intervals and flight routes and range areas were obtained through
mapping of successive locations and roost fixes. The procedure of
We performed active searches for the signal and used triangulation techniques to obtain locations (Jacob and Rudran, 2003) using
a radio-receiver model TR-5 (Telonics Inc.) coupled to a two-
Table 1
Summary of results obtained per species. KF 95% – Fixed Kernel estimates of range use with 95% of samples; % Use – Percentage of foraging area composed by the Restored Area
habitat; Commuting distance – Mean distance traveled between roosting and foraging areas. Individuals insufficiently sampled for analysis are highlighted in bold.
Species/individuals
Sex
Season
Days sampled
Obtained locations
Day roosts
KF 95% (ha)
% Use
Commuting distance (m)
Carollia perspicillata
1
2
3
4
5
6
7
8
9
10
11
12
Mean ± SD
Female
Male
Male
Male
Male
Female
Male
Female
Female
Female
Female
Female
Dry
Dry
Wet
Wet
Wet
Wet
Wet
Wet
Wet
Dry
Dry
Dry
4
5
3
4
4
7
5
6
7
8
4
4
58
31
6
23
25
21
16
19
17
27
17
25
0
1
0
2
1
2
2
1
2
1
0
0
29.63
16.33
–
15.38
54.43
17.47
23.84
26.85
45.107
40.17
79.15
28.74
34.2 ± 19.4
46.27
29.84
–
23
14.29
38.2
29.45
49.61
25.38
28.33
37.8
34.02
32.3 ± 10.2
–
722.2
–
495.9
617.6
198
262
357.7
299.1
958.7
–
–
488.9 ± 262.1
Artibeus lituratus
1
2
3
4
5
6
7
8
9
10
11
12
Mean ± SD
Female
Female
Female
Male
Male
Male
Male
Male
Female
Male
Male
Male
Dry
Wet
Wet
Wet
Wet
Wet
Wet
Wet
Wet
Dry
Dry
Dry
6
4
8
5
3
5
6
3
5
6
8
4
17
18
16
27
15
15
9
17
25
15
20
24
4
1
0
2
0
1
0
0
1
1
1
2
73.64
30.01
154.16
57.35
6.7
136.03
–
172.18
389.72
77.94
61.53
90.1
124.3 ± 103.8
17.98
45.53
41.92
44.11
–
23.26
–
35.77
29.06
20.63
30.88
26.45
31.56 ± 9.9
788.1
2053.2
–
2001
–
1295.6
–
–
1076.2
650.9
987
418.2
1158.8 ± 598.6
3. Responses to food resource availability
The overall fruit production of plant species that comprise the
ets of the bats was continuous, with some species alternating
that forest remnants (mostly riparian forests) act as a source o
new colonist species and individuals (Turner and Corlett, 1996
Lindenmayer et al., 2008), assisting the gradual recolonization o
restored areas. A similar pattern of habitat selection was observed
. 2. Relationship between habitat use by Artibeus liturartus (A) and Carollia perspicillata (B) (as observed in the range area of both species) and habitat availability in th
dscape used by each species (accessed with 100%MCP – see text for description).
✓ Testes de Randomização – uso do espaço em % diferente á disponível
✓ Área restaurada – maior % de uso e maior % probabilidade de uso
Fig. 3. Estimates of fruit availability of the three plant populations identified as
major items in the diet of both bats species in the study area.
Fig. 4. Box-plot comparing mean commuting distance from roosts to foraging areas
for Carollia perspicillata between periods with and without the presence of ripe
fruits of Piper aduncum in the population.
gest that Carollia actively selects Piper species wh
(Fleming and Heithaus, 1986; Thies and Kalko, 20
et al., 2012).
On the other hand, we failed to support other pr
lated to direct responses in the use of restored areas
by A. lituratus and for foraging by both species, to th
of each specific food item in these habitats. This non
tionship between the availability of specific food item
ing movement in restored areas could indicate that
responding to food availability in other habitats of th
While this is a valid alternative explanation, we hav
that Restored areas are being used as their main forag
study and Silveira et al., 2011). Considering that overa
of food resource was relatively constant (fruiting p
alternated but maintained overall production; Fig. 3)
to assume that constant use of the restored area for
flects this constancy in overall food availability. Stud
locations have shown feeding plasticity for both sp
and Morellato, 1994; Passos et al., 2003; Mello et al., 2
et al., 2011), despite of the purported ‘‘preference
phyllostomid (Mello et al., 2011). Our results may
how this plasticity reflects on foraging behavior (Flem
haus, 1986) and, consequently, on the use of the resto
we initially hypothesized. In a recently restored area
planted species are not mature enough to bear fruits, t
cies are adapting their diets to what is available, and, c
using space accordingly. From the restoration view
aduncum
plant species arePiper
effective
in continuously attracting a
these frugivores, contributing to the initial recovery o
this area (Silveira et al., 2011).
4.2. Movement patterns
in foraging movements, with Restored areas being the most frequently used foraging habitat for both species. Both these aspects
of our data represent evidence that the restored forest habitat is
contributing to the persistence of A. lituratus and C. perspicillata
populations in the landscape and extending their distribution.
There is a lack of studies directly estimating ho
range areas for A. lituratus, but some studies report
over large distances (Morison, 1980; Menezes Jr. et
well as low fidelity to local forest patches (Bianconi
13 abrigos
11 abrigos
1)  Florestais Secundárias
AL – 9 abrigos
CP – 6 abrigos
2) Área Restaurada
AL – 4 abrigos
CP – 5 abrigos
è
Fidelidade no uso da área para abrigo
Aumento na complexidade estrutural e oferta de recursos
Rápida colonização por
morcegos frugívoros
(estágios iniciais)
Aumenta possibilidade de aporte
de semestes alóctones
Conexão de espécies de plantas entre diferentes unidades
da paisagem – fluxo gênico e aumento na biodiversidade
Qualidade da matriz adjacente
a área restaurada
Utilização de técnicas alternativas para atração de morcegos frugívoros
RESEARCH ARTICLE
Use of Fruit Essential Oils to Assist Forest
Regeneration by Bats
Gledson V. Bianconi,1,2,3 Urubatan M. S. Suckow,4 Ariovaldo P. Cruz-Neto,1
and Sandra B. Mikich5
Abstract
revealed a huge potential for dispersion of a vast amount
of seeds from different plant species at the IU. Although
Agradecimentos
•  International Paper
•  Secretaria do Meio Ambiente SP
•  Programa de Políticas Públicas – FAPESP
Estabelecimento de parâmetros de
avaliação e monitoramento para
reflorestamento.
•  Estagiários (as)
•  The “Ana’s”
(ACM Martins e ACT Cançado)
• 
Marcio Port-Carvalho
Daniel H. Homem
Simone Godoi
Elisabeth Mandetta
•  Maurício Silveira & Leonardo Trevelin