morcegos e áreas restauradas: uma via de mão dupla · morcegos e áreas restauradas: uma via de...

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

.

Morcegos e Áreas Restauradas: Uma Via de Mão Dupla

Simpósio: Morcegos como pilares da natureza

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

Banco de sementes Chuva de sementes

Anemocórica Zoocórica

Qual a importância dos morcegos frugívoros para o sucesso de

projetos de restauração?

Contribuição significativa para o aporte de sementes alóctones

Author's personal copy

Original article

Frugivory by phyllostomid bats (Mammalia: Chiroptera) in a restoredarea in Southeast Brazil

Maurício Silveira a,1, Leonardo Trevelin b, Marcio Port-Carvalho c, Simone Godoi d,Elizabeth Neuenhaus Mandetta a, Ariovaldo P. Cruz-Neto b,*

aDepartamento de Botânica, Universidade Estadual Paulista (UNESP), Av. 24-A, 1515, 13506-900 Rio Claro, São Paulo, BrazilbDepartamento de Zoologia, Universidade Estadual Paulista (UNESP), Av. 24-A, 1515, 13506-900 Rio Claro, São Paulo, BrazilcDivisão de Florestas e Estações Experimentais, Instituto Florestal, Av. Rodrigues Alves 38-25, 17013-000 Bauru, São Paulo, BrazildDepartamento de Botânica, Universidade de São Paulo (USP), Rua do Matão 277, Caixa Postal 1461, 05422-970 São Paulo, SP, Brazil

a r t i c l e i n f o

Article history:Received 26 January 2010Accepted 10 November 2010Available online 13 December 2010

Keywords:Seed dispersalDietFrugivorous batsEcological restorationSemi deciduous forests

a b s t r a c t

We studied the potential contribution of frugivorous bats to the reestablishment of vegetational diversityin a restored area. We analysed the diets of the bat species and the differences between them in theconsumption of fruits of autochtonous and allochthonous species. Planted (autochtonous) species werethe basis of diets, especially Solanum mauritianum and Cecropia pachystachya, whereas for allochthonousspecies we found that Piperaceae to be of particular importance. Carollia perspicillata was the main seeddisperser for allochthonous species, and potentially the most important bat in the promotion of vege-tation diversity in the study area. Our results suggest that frugivorous bats are especially important in thereestablishment of vegetation in disturbed areas, and that restorarion efforts should focus on theplanting of different zoochorous species that would guarantee a high year-round fruit production,thereby facilitating natural plant reestablishment by frugivorous bats in regenerating areas.

! 2010 Elsevier Masson SAS. All rights reserved.

1. Introduction

Ecological restoration is an intentional activity that initiates oraccelerates the recovery of an ecosystem with respect to its health,integrity and sustainability (Young et al., 2005; Van Andel andGrootjans, 2006). The ultimate goal of any restoration project isto return ecosystems form, function and process to a condition that,as close as possible, resembles those found prior to the effectsinduced by man-made activities (Engel and Parrotta, 2003).Moreover, as far as the recovering of local biodiversity is concerned,restoration projects attempt to create sustainable conditions thatwould allow for the reproduction and genetic diversity of thespecies concerned (Young, 2000).

The recovery, sustainability and maintenance of biodiversity inrestored or naturally regenerated areas depends, to a large extent,on the recruitment of new individuals and species either from theseed bank or from seed rain (Holl, 1999; Grombone-Guaratini and

Rodrigues, 2002; Zamora and Montagnini, 2007). Seed raininvolves either the recruitment of seeds from planted trees(autochtonous seeds), or from colonist trees (i.e. allochthonousseeds from trees not used in the original restoration project) fromthe surrounding matrix (Martinéz-Ramos and Soto-Castro, 1993;Martínez-Garza and González-Montagut, 2002). By limiting theincrease in local biodiversity, the absence of allochthonous seeds isregarded as one of the main factors curtailing the success of forestregeneration, both for natural and for restored areas (Finegan andDelgado, 2000; Zimmerman et al., 2000).

At least in the Neotropical quarters, the seed rain of restoredareas is dominated by windedispersed (anemochorous) seeds(Augspurger and Franson, 1988; Grombone-Guaratini andRodrigues, 2002; Barbosa and Pizo, 2006). A recent study,however, demonstrated that seed limitation (defined as the failureof seeds to arrive at suitable sites Muller-Landau et al., 2002) washigher for anemochorous seeds than for animal dispersed (zoo-chorous) seeds, and that limitation was higher for autochtonousthan for allochthonous seeds (Barbosa and Pizo, 2006). From this,and the widely recognized importance of vertebrates in mediatingseed dispersal in the tropics (Howe and Smallwood, 1982), it isclear that patterns of animal mediated seed dispersal are animportant ecological component that should be taken intoaccount in regeneration programs. The incorporation of the

* Corresponding author.E-mail address: [email protected] (A.P. Cruz-Neto).

1 Present address: Departamento de Biologia, Universidade Federal de MatoGrosso do Sul (UFMS), Cidade Universitária s/n, 79070-900 Campo Grande, MatoGrosso do Sul, Brazil.

Contents lists available at ScienceDirect

Acta Oecologica

journal homepage: www.elsevier .com/locate/actoec

1146-609X/$ e see front matter ! 2010 Elsevier Masson SAS. All rights reserved.doi:10.1016/j.actao.2010.11.003

Acta Oecologica 37 (2011) 31e36


Original article

Frugivory by phyllostomid bats (Mammalia: Chiroptera) in a restoredarea in Southeast Brazil

Maurício Silveira a,1, Leonardo Trevelin b, Marcio Port-Carvalho c, Simone Godoi d,Elizabeth Neuenhaus Mandetta a, Ariovaldo P. Cruz-Neto b,*

aDepartamento de Botânica, Universidade Estadual Paulista (UNESP), Av. 24-A, 1515, 13506-900 Rio Claro, São Paulo, BrazilbDepartamento de Zoologia, Universidade Estadual Paulista (UNESP), Av. 24-A, 1515, 13506-900 Rio Claro, São Paulo, BrazilcDivisão de Florestas e Estações Experimentais, Instituto Florestal, Av. Rodrigues Alves 38-25, 17013-000 Bauru, São Paulo, BrazildDepartamento de Botânica, Universidade de São Paulo (USP), Rua do Matão 277, Caixa Postal 1461, 05422-970 São Paulo, SP, Brazil


Article history:Received 26 January 2010Accepted 10 November 2010Available online 13 December 2010

Keywords:Seed dispersalDietFrugivorous batsEcological restorationSemi deciduous forests

a b s t r a c t

We studied the potential contribution of frugivorous bats to the reestablishment of vegetational diversityin a restored area. We analysed the diets of the bat species and the differences between them in theconsumption of fruits of autochtonous and allochthonous species. Planted (autochtonous) species werethe basis of diets, especially Solanum mauritianum and Cecropia pachystachya, whereas for allochthonousspecies we found that Piperaceae to be of particular importance. Carollia perspicillata was the main seeddisperser for allochthonous species, and potentially the most important bat in the promotion of vege-tation diversity in the study area. Our results suggest that frugivorous bats are especially important in thereestablishment of vegetation in disturbed areas, and that restorarion efforts should focus on theplanting of different zoochorous species that would guarantee a high year-round fruit production,thereby facilitating natural plant reestablishment by frugivorous bats in regenerating areas.

! 2010 Elsevier Masson SAS. All rights reserved.

1. Introduction

Ecological restoration is an intentional activity that initiates oraccelerates the recovery of an ecosystem with respect to its health,integrity and sustainability (Young et al., 2005; Van Andel andGrootjans, 2006). The ultimate goal of any restoration project isto return ecosystems form, function and process to a condition that,as close as possible, resembles those found prior to the effectsinduced by man-made activities (Engel and Parrotta, 2003).Moreover, as far as the recovering of local biodiversity is concerned,restoration projects attempt to create sustainable conditions thatwould allow for the reproduction and genetic diversity of thespecies concerned (Young, 2000).

The recovery, sustainability and maintenance of biodiversity inrestored or naturally regenerated areas depends, to a large extent,on the recruitment of new individuals and species either from theseed bank or from seed rain (Holl, 1999; Grombone-Guaratini and

Rodrigues, 2002; Zamora and Montagnini, 2007). Seed raininvolves either the recruitment of seeds from planted trees(autochtonous seeds), or from colonist trees (i.e. allochthonousseeds from trees not used in the original restoration project) fromthe surrounding matrix (Martinéz-Ramos and Soto-Castro, 1993;Martínez-Garza and González-Montagut, 2002). By limiting theincrease in local biodiversity, the absence of allochthonous seeds isregarded as one of the main factors curtailing the success of forestregeneration, both for natural and for restored areas (Finegan andDelgado, 2000; Zimmerman et al., 2000).

At least in the Neotropical quarters, the seed rain of restoredareas is dominated by windedispersed (anemochorous) seeds(Augspurger and Franson, 1988; Grombone-Guaratini andRodrigues, 2002; Barbosa and Pizo, 2006). A recent study,however, demonstrated that seed limitation (defined as the failureof seeds to arrive at suitable sites Muller-Landau et al., 2002) washigher for anemochorous seeds than for animal dispersed (zoo-chorous) seeds, and that limitation was higher for autochtonousthan for allochthonous seeds (Barbosa and Pizo, 2006). From this,and the widely recognized importance of vertebrates in mediatingseed dispersal in the tropics (Howe and Smallwood, 1982), it isclear that patterns of animal mediated seed dispersal are animportant ecological component that should be taken intoaccount in regeneration programs. The incorporation of the

* Corresponding author.E-mail address: [email protected] (A.P. Cruz-Neto).

1 Present address: Departamento de Biologia, Universidade Federal de MatoGrosso do Sul (UFMS), Cidade Universitária s/n, 79070-900 Campo Grande, MatoGrosso do Sul, Brazil.

Contents lists available at ScienceDirect

Acta Oecologica

journal homepage: www.elsevier .com/locate/actoec

1146-609X/$ e see front matter ! 2010 Elsevier Masson SAS. All rights reserved.doi:10.1016/j.actao.2010.11.003

Acta Oecologica 37 (2011) 31e36

2011


conceptual background of animaleplant interactions into resto-ration programs has great potential to improve the design,execution and evaluation of such programs (Wunderle Jr., 1997;Holl, 1998; Silva, 2003; Martínez-Garza and Howe, 2003).

Although the theoretical and practical aspects of restorationprograms are well developed in Brazil (Barbosa et al., 2003;Kageyama et al., 2003), the importance of frugivory for the prac-tical implementation of such programs has only been consideredon theoretical basis (Silva, 2003; Rodrigues and Gandolfi, 2000).The New World fruit-eating bats (Chiroptera: Phyllostomidae) aregoodmodels for such studies.Within Neotropical bats assemblages,fruit-eating species constitute the dominant andmost diverse guildin terms of feeding habits (Kalko, 1998; Medellin et al., 2000;

Dumont, 2003; Giannini and Kalko, 2004; Mello, 2009). Throughseed dispersal, fruit-eating phyllostomid bats play a crucial role themaintenance of tropical ecosystem dynamics (Fleming andHeithaus, 1981; Medellin et al., 2000; Bernard and Fenton, 2007;Henry et al., 2007; Medellin and Gaona, 1999; Galindo-Gonzálezet al., 2000; Arteaga et al., 2006; Henry and Jouard, 2007).Indeed, methods for attracting fruit-eating bats to degraded areasare currently being considered as a mechanism for their effectiverestoration (Bianconi et al., 2007; Kelm et al., 2008).

In this paper we analyse the potential contribution of fruit-eating phyllostomid bats to the input of allochthonous seeds ina restored area in Southeast Brazil. We address two basic questions:a) what are the diets of the fruit-eating bat species already resident

Fig. 1. Localization and general characterization of the RPPN São Marcelo in São Paulo State, Brazil.

M. Silveira et al. / Acta Oecologica 37 (2011) 31e3632

RPPN Parque São Marcelo (International Paper – Mogi Guaçu, SP)

2002/2003 – Programa restauração # 2 •  240 ha – Resolução SMA 47/2003 •  101 espécies de plantas


3. Results

We mist-netted 542 individuals of eight species of predomi-nantly or exclusively frugivores phyllostomid bats during our study,with the exception of Glossophaga soricina which also feeds onnectar and pollen, and Phyllostomus discolor, considered anomnivorous species, both with records of frugivory in other regions(Willig et al., 1993; Zortéa, 2003; Sato et al., 2008). The mostcommon species were, in ranked order, Artibeus lituratus, Platyr-rhinus lineatus, Sturnira lilium and Carollia perspicillata (Table 2). Weobtained a total of 184 fecal samples from a total of six species. Ofthese, 182 contained plant materials, and two consisted entirely ofarthropods remains. The great majority of fecal samples containedonly one type of seeds (91%) and the twomost common bat speciescontributed with the majority of fecal samples (Table 3). From the182 samples, we identified 8 different morphotypes of seeds fromplants of at least 4 families, and identified 6 to genus level or below(Table 3). The most common genus consumed by bats was Solanum(60% of samples), Cecropia (20% of samples), Piper (8.1% of samples)and Ficus (7.6% of samples). Solanum was consumed in highestproportion by the four most common bats species. The relativecontribution of the other plant species to the diet varied betweenthe bat species (Fig. 2).

Three allochthonous species were recorded in the diet of thebats: Piper aduncum and Photomorpha umbellata (both Piperaceaee18 samples), and Ficus sp.1 (Moraceae e five samples). The maindispersers of allochthonous seeds were A. lituratus and C.

perspicillata. Together, these two species were responsible for 82.6%of the total samples containing allochthonous seeds. There was,however, a difference between these two species in theirconsumption of allochthonous vs. autochtonous seeds (c2¼16.43df¼ 1 p< 0.05; Fig. 3), with the allochthonous seeds being found in35.7% of the total fecal samples for C. perspicillata, whilst they werefound only in 5.6% of the total fecal samples for A. lituratus.

Despite not having been planted as part of the restorationprogram, a few young individuals of P. aduncum and P. umbellata hadestablished in the restored area, but none presented fruit productionduring this study. Even so, seeds fromboth specieswere encounteredin bats feces collected in various months, reaffirming the allochtho-nous nature of this sample. In contrast, all autochtonous speciesconsumed by bats during our study produced fruit in the restored

Table 2List of fruit-eating phyllostomid bats captured within the restored area during thestudy period. Numbers indicate the total number of individuals of each speciescaptured during the study and does not include recaptures.

Species Number of captures (%)

Artibeus lituratus (Al) 258 48.8Platyrrhinus lineatus (Pl) 81 15.3Sturnira lilium (Sl) 80 15.1Carollia perspicillata (Cp) 77 14.6Glossophaga soricina (Gs)a 24 4.5Vampyressa pusilla (Vp) 5 0.9Pygoderma bilabiatum (Pb) 3 0.6Phyllostomus discolor 1 0.2

Total 529 100

a Although G. soricina has a diet mostly based on nectar and pollens, it wasincluded in this study as we found seeds remain in its feces.

Table 3Number of faecal samples collected for each individual bat within the restored areacontaining seeds from a specific plant species. Feaces that contained seeds froma single species were treated as a single sample, while feaces that contained seedsfrom two or more species were treated as different samples. For abbreviations of batspecies see Table 1.

Plants consumed(family/species)

Bat species

Al Cp Gs Pl Sl Vp Total

CecropiaceaeCecropia pachystachya 25 2 2 5 3 37MoraceaeFicus guaranitica 4 4 1 9Ficus sp1a 2 1 1 1 5PiperaceaePiper aduncuma 2 11 2 15Photomorpha umbellataa 3 3SolanaceaeSolanum mauritianum 36 25 1 19 30 111Non-Identified 2 2

Total 71 42 3 29 36 1 182

a Seeds from allochtonous trees (plants not originally planted in the restorationprogram).

0

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Cp Fsp Pa Pu Sm NI

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Plant SpeciesCp Fsp Pa Pu Sm NI

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Artibeus lituratus Carollia perspicillata

Sturnira liliumPlathyrrinus lineatus

Fig. 2. Frequency of occurrence (%) of different plant species in fecal samples of the batsArtibeus lituratus, Carollia perspicillata, Sturnira lilium and Platyrrhinus lineatus. Cp e

Cecropia pachystachya. Fspe Ficus spp. Pae Piper aduncum. Pue Photomorpha umbellata.Sm e Solanum mauritianum. NI e Non-identified morphotype.

sepmaSforeb

muN

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70


Fig. 3. Number of fecal samples containing autochtonous (closed bars) and allochth-onous (open bars) seeds for Artibeus lituratus and Carollia perspicillata.


Fotos: www.casadosmorcegos.org


in the restored area? and b) how much of this diet is composed offruits from coloniser species (i.e. from trees not used in the resto-ration programs)? By answering these two questions, we hoped todetermine the importance of phyllostomid bats for the input ofcolonist seeds and, hence, improvement of the biodiversity to therestored area.

2. Materials and methods

2.1. Study area

This study was carried out in a restored area within the ReserveParque São Marcelo (RPSM), Mogi-Guaçu municipality, São PauloState, Southeast Brazil (22!220S, 46!580W). During this study, totalannual precipitation was 1062.5 mm, varying from a minimum of6.6 mm (June) to a maximum of 215.9 mm (March). Meantemperature varied between 24.1 !C (January) and 16.5 !C (June).The RPSM was originally covered by typical semidecidous forests(Kronka et al., 2005), but has an intensive history of humanexploitation, first by coffee plantations and cattle grazing and, morerecently, by eucalyptus plantation. The current land use patterncomprises of: semidecidous forest remnants (30%), eucalyptusplantations (38%), anthropogenic land use (5%), with heteroge-neous reforested areas comprising 27% of the area’s 987 ha (Fig. 1).

One of such areas was used in a restoration program in 1996. Inthis program, 23 native species were planted in different modules,each containing pioneer and late-successional species. Unfortu-nately, no study was conducted on the forest dynamics after theimplementation of this program. Latter, in 2002, an area of 240 hawas set aside for new restoration program, which followed theguidelines proposed by the Sao Paulo State EnvironmentalSecretary (resolution SMA 47/2003 e www.ambiente.sp.gov.br/contAmbientalLegislacaoAmbiental.php). Briefly, 101 differentplant species, representing a mix of pioneer and late-successionalspecies, with different dispersal syndromes were used (a list of thespecies is available from the corresponding author upon request).From the original list of species used, 12 are reported to beconsumed by bats (Table 1). The planting was carried out in 40parcels (36 " 62.5 m) and in each parcel the same proportion ofplants, with respect to their ecological groups (pioneer or late-successional species) were used. Currently, the area presents itself

on an early-successional development stage, with a discontinuouscanopy of about 4e5 m high and a diverse array of species onreproductive phase.

2.2. Bat capture and dietary analysis

We mist-netted bats for four consecutive nights each month,from September 2005 to August 2006 (except May). We usedbetween five and eight mist nets each night (9 " 2.5 m and12 " 2.5 m), which were opened at approx. 18:00 h and thenregularly checked at 30min intervals for the next 6 h. The nets wereplaced in different locations within the study area, and an effortwas made not to repeat locations within a given month. Overall oursampling effort, calculated according to Straube and Bianconi(2002)’s methodology, totalled 36,588 h m2. We held capturedbats in cloth bags for at least 1 h to collect fecal samples. Allcollected fecal samples were then individually identified and storeddry in a freezer for latter analysis. We also placed a plastic sheetbeneath each deployed net in order to collected such pieces of fruitsas might be dropped by bats upon being caught. Before release,animals wereweighed, sexed, their forearmmeasured, and markedwith a numbered aluminum tag placed in the forearm. We identi-fied the bat species using Nowak (1994) and Emmons and Feer(1997).

To analyse the dietary patterns, we rinsed the frozen fecalsamples with distilled water and analysed the contents under a 2"magnifier (Zeiss Inc.). We analysed the samples for the followingfood items: seeds, pulp, flowers, pollen and arthropod parts. Wetried to identify the fruit food items to the lowest possible taxo-nomic level, by comparing the samples with an existing referencecollection based on fruits collected within the study area.

We considered only the presence or absence or each item ina single fecal sample. To analyse the proportion of each food item inthe diet of a given bat species, we calculated the proportion of eachitem in relation to the total number of samples observed for thatspecies (Passos et al., 2003; Mello et al., 2004). To analyse thedifference in the consumption of autochtonous and allochthonousfruits, we classified autochtonous seeds as being those from fruitsof tree species originally used in the restoration program, whileallochthonous seeds were those fruits from tree species that werenot part of the 101 species originally used for the restorationprograms. The difference in the consumption of autochtonous andallochthonous species by the fruit-eating bats were analysed bya c2 test. The association between the variables “resource” and “batspecies” is indicative of the potential of different bat species todisperse allochthonous seeds into the restored areas as well as anindicative of the degree by which the bats depend on autochtho-nous plant species as food resources.

2.3. Fruit availability

We carried out a fruit availability survey between March 2005and February 2006, aiming to track the availability of speciesconsumed by bats in the restored area. This data was used toevaluate if individuals of the autochthonous species consumed bybats were producing fruits during the sampling periods. If theywere not, we assumed that bats to be consuming fruits from indi-viduals of these species located outside the restored area. Plantspecies that did not produce fruits were not included in this study.Fruiting of chiropterocoric species planted in the area (Table 1) wasassessed monthly, and we registered presence or absence of ripefruits on each sampled individual. Number of marked individualsfor each species was based on its availability in sampled plots, andvaried from 33 individuals of Solanum mauritianum to one indi-vidual of Ficus citrifolia.

Table 1Planted species reported to be consumed by bats in a restored area.

Plant species Successional stage Fruiting

AraliaceaeDendropanax cuneatum Decne & Planch. Late successionalCecropiaceaeCecropia pachystachya Trec. Pioneer XFabaceaeInga uruguensis Hooker et Arnot Pioneer XCopaifera langsdorfii Desf. Late successionalHolocalyx balansae Mich. Late successionalMoraceaeFicus citrifolia Schodat Pioneer XMaclura tinctoria (L.) D. Don ex Steud. Late successionalMyrtaceaeEugenia uniflora L. Late successional XPsidium guajava L. Pioneer XSapindaceaeSapindus saponaria L. Late successionalSolanaceaeSolanum mauritianum Scop. Pioneer XSterculiaceaeGuazuma ulmifolia Lam. Pioneer X

Identification of plant species was carried out by specialists from The BotanicalInstitute of Sao Paulo, Brazil.

M. Silveira et al. / Acta Oecologica 37 (2011) 31e36 33

2005/2006


3. Results








Total 529 100




Bat species



Total 71 42 3 29 36 1 182


0

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80

100

0

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Cp Fsp Pa Pu Sm NI

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ecneruccOfo

ycneuqerF

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0

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sepmaSforeb

muN

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60

70




Solanum mauri+anum


3. Results








Total 529 100




Bat species



Total 71 42 3 29 36 1 182


0

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80

100

0

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Cp Fsp Pa Pu Sm NI

)%(

ecneruccOfo

ycneuqerF

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100


0

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100





sepmaSforeb

muN

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70




Piper aduncum

Consumo de plantas alóctones Artibeus e Carollia – 87%

33%

6%

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?

A. lituratus (n = 10)

C. perspicillata (n = 11)

2008

•  5 sessões de 4 a 8 dias •  Estação seca e chuvosa

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


Use of space by frugivorous bats (Chiroptera: Phyllostomidae) in a restoredAtlantic forest fragment in Brazil

Leonardo C. Trevelin a,⇑, Maurício Silveira b,1, Marcio Port-Carvalho c, Daniel H. Homem a,Ariovaldo P. Cruz-Neto a

a Departmento de Zoologia, Universidade Estadual Paulista (UNESP), Av. 24-A, 1515, CEP 13506-900, Rio Claro, SP, Brazilb Departamento de Botânica, Universidade Estadual Paulista (UNESP), Av. 24-A, 1515, CEP 13506-900, Rio Claro, SP, Brazilc Divisão de Florestas e Estações Experimentais – Instituto Florestal, Av. Rodrigues Alves 38-25, CEP 17013-000, Bauru, São Paulo, Brazil


Article history:Received 6 April 2012Received in revised form 7 November 2012Accepted 9 November 2012

Keywords:ArtibeusCarolliaDay roostHabitat useRadio-telemetryRange area

a b s t r a c t

We studied patterns in the use of space for foraging and roosting by two frugivorous bat species in a five-year-old restored Atlantic forest located in a fragmented landscape in southeastern Brazil. Ten individualsof Carollia perspicillata and eleven individuals of Artibeus lituratus were monitored through radio-telemetryin five sampling sessions. Each session lasted 3–8 days for each individual, with an average of 25.4 ± 10locations for each C. perspicillata individual and 19 ± 4.4 for each A. lituratus individual. We described anaverage range of 124.4 ha and an average commuting distance of 1158.8 m for A. lituratus and an averagerange and commuting distance of 32 ha and 489 m, respectively, for C. perspicillata. We demonstrated aconsistent pattern in habitat use and movements for both studied species, where they strictly used forests(restored or not) for day roosting, roosting in the foliage of trees located only in secondary forest remnantsand restored areas, while restored areas were their main feeding habitat. We demonstrate that newlyrestored forests can be readily incorporated as foraging and roosting habitats by these species, and thatC. perspicillata alters its roosting behavior in relation to preferred food availability. These results, whencombined with data on the diet of the studied species, show consistent evidence of the potential that batshave to improve species diversity of anthropogenic plantings with their own natural seed dispersal.

! 2012 Elsevier B.V. All rights reserved.

1. Introduction

The evaluation of the success of restoration projects is a strate-gic initiative and should be based on the monitoring of indicatorsof progress toward predefined goals (Holl and Aide, 2011). Thispractice, however, is strongly biased toward the use of only vege-tational parameters as indicators of progress, and a common find-ing in studies of Neotropical reforestation sites is that newcolonizing plant species fail to reach and become established in re-stored areas, especially in highly fragmented landscapes (Holl,1999; Rodrigues et al., 2009).

Animal-mediated seed dispersal is the prevailing form of seeddissemination in tropical forests (Howe and Smallwood, 1982),

and much of the potential of these animals to visit and bringnew seeds to revegetated sites depends on the availability ofsource areas (of plants and animals) in the landscape and the ani-mal’s efficiency in moving between these areas (Wunderle Jr.,1997). Isolation is a response to the interaction between landscapestructure and dynamics (including local-scale site characteristics)with specific aspects of animal behavior (Dewalt et al., 2003; Fah-rig, 2003; Fischer and Lindenmayer, 2007). Therefore, in the devel-opment of reliable indicators of the re-establishment of seed flowto non-isolated restored areas and, consequently, the successfulrestoration of successional dynamics, it is of paramount impor-tance to measure the faunal contribution to this process (Lindell,2008).

New World fruit-eating bats (Chiroptera: Phyllostomidae) areamong the most abundant seed dispersers in Neotropical forests,and because they include a diverse array of early-successionalplant species in their diet, they are regarded as playing an impor-tant role in the successional dynamics of these forests (Medellinand Gaona, 1999; Galindo-Gonzalez et al., 2000; Muscarella andFleming, 2007). As highly vagile animals, some authors have ar-gued that many species of bats may persist under conditions thatare limiting to other mammals (Bernard and Fenton, 2003;

0378-1127/$ - see front matter ! 2012 Elsevier B.V. All rights reserved.http://dx.doi.org/10.1016/j.foreco.2012.11.013

⇑ Corresponding author. Present address: Coordenação de Zoologia, MuseuParaense Emílio Goeldi, Av. Perimetral 1901, CEP 66077-530, Belém, Pará, Brazil.Tel.: +55 091 3075 6108.

E-mail addresses: [email protected] (L.C. Trevelin), [email protected] (M. Silveira), [email protected] (M. Port-Carvalho), [email protected] (D.H. Homem), [email protected] (A.P. Cruz-Neto).

1 Present address: Departamento de Biologia, Universidade Federal do Mato Grossodo Sul (UFMS), Cidade Universitária s/n, CEP 79070-900, Campo Grande, Mato Grossodo Sul, Brazil.

Forest Ecology and Management 291 (2013) 136–143

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Use of space by frugivorous bats (Chiroptera: Phyllostomidae) in a restoredAtlantic forest fragment in Brazil

Leonardo C. Trevelin a,⇑, Maurício Silveira b,1, Marcio Port-Carvalho c, Daniel H. Homem a,Ariovaldo P. Cruz-Neto a

a Departmento de Zoologia, Universidade Estadual Paulista (UNESP), Av. 24-A, 1515, CEP 13506-900, Rio Claro, SP, Brazilb Departamento de Botânica, Universidade Estadual Paulista (UNESP), Av. 24-A, 1515, CEP 13506-900, Rio Claro, SP, Brazilc Divisão de Florestas e Estações Experimentais – Instituto Florestal, Av. Rodrigues Alves 38-25, CEP 17013-000, Bauru, São Paulo, Brazil


Article history:Received 6 April 2012Received in revised form 7 November 2012Accepted 9 November 2012

Keywords:ArtibeusCarolliaDay roostHabitat useRadio-telemetryRange area

a b s t r a c t

We studied patterns in the use of space for foraging and roosting by two frugivorous bat species in a five-year-old restored Atlantic forest located in a fragmented landscape in southeastern Brazil. Ten individualsof Carollia perspicillata and eleven individuals of Artibeus lituratus were monitored through radio-telemetryin five sampling sessions. Each session lasted 3–8 days for each individual, with an average of 25.4 ± 10locations for each C. perspicillata individual and 19 ± 4.4 for each A. lituratus individual. We described anaverage range of 124.4 ha and an average commuting distance of 1158.8 m for A. lituratus and an averagerange and commuting distance of 32 ha and 489 m, respectively, for C. perspicillata. We demonstrated aconsistent pattern in habitat use and movements for both studied species, where they strictly used forests(restored or not) for day roosting, roosting in the foliage of trees located only in secondary forest remnantsand restored areas, while restored areas were their main feeding habitat. We demonstrate that newlyrestored forests can be readily incorporated as foraging and roosting habitats by these species, and thatC. perspicillata alters its roosting behavior in relation to preferred food availability. These results, whencombined with data on the diet of the studied species, show consistent evidence of the potential that batshave to improve species diversity of anthropogenic plantings with their own natural seed dispersal.

! 2012 Elsevier B.V. All rights reserved.

1. Introduction

The evaluation of the success of restoration projects is a strate-gic initiative and should be based on the monitoring of indicatorsof progress toward predefined goals (Holl and Aide, 2011). Thispractice, however, is strongly biased toward the use of only vege-tational parameters as indicators of progress, and a common find-ing in studies of Neotropical reforestation sites is that newcolonizing plant species fail to reach and become established in re-stored areas, especially in highly fragmented landscapes (Holl,1999; Rodrigues et al., 2009).

Animal-mediated seed dispersal is the prevailing form of seeddissemination in tropical forests (Howe and Smallwood, 1982),

and much of the potential of these animals to visit and bringnew seeds to revegetated sites depends on the availability ofsource areas (of plants and animals) in the landscape and the ani-mal’s efficiency in moving between these areas (Wunderle Jr.,1997). Isolation is a response to the interaction between landscapestructure and dynamics (including local-scale site characteristics)with specific aspects of animal behavior (Dewalt et al., 2003; Fah-rig, 2003; Fischer and Lindenmayer, 2007). Therefore, in the devel-opment of reliable indicators of the re-establishment of seed flowto non-isolated restored areas and, consequently, the successfulrestoration of successional dynamics, it is of paramount impor-tance to measure the faunal contribution to this process (Lindell,2008).

New World fruit-eating bats (Chiroptera: Phyllostomidae) areamong the most abundant seed dispersers in Neotropical forests,and because they include a diverse array of early-successionalplant species in their diet, they are regarded as playing an impor-tant role in the successional dynamics of these forests (Medellinand Gaona, 1999; Galindo-Gonzalez et al., 2000; Muscarella andFleming, 2007). As highly vagile animals, some authors have ar-gued that many species of bats may persist under conditions thatare limiting to other mammals (Bernard and Fenton, 2003;

0378-1127/$ - see front matter ! 2012 Elsevier B.V. All rights reserved.http://dx.doi.org/10.1016/j.foreco.2012.11.013

⇑ Corresponding author. Present address: Coordenação de Zoologia, MuseuParaense Emílio Goeldi, Av. Perimetral 1901, CEP 66077-530, Belém, Pará, Brazil.Tel.: +55 091 3075 6108.

E-mail addresses: [email protected] (L.C. Trevelin), [email protected] (M. Silveira), [email protected] (M. Port-Carvalho), [email protected] (D.H. Homem), [email protected] (A.P. Cruz-Neto).

1 Present address: Departamento de Biologia, Universidade Federal do Mato Grossodo Sul (UFMS), Cidade Universitária s/n, CEP 79070-900, Campo Grande, Mato Grossodo Sul, Brazil.

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

2013


conceptual background of animaleplant interactions into resto-ration programs has great potential to improve the design,execution and evaluation of such programs (Wunderle Jr., 1997;Holl, 1998; Silva, 2003; Martínez-Garza and Howe, 2003).

Although the theoretical and practical aspects of restorationprograms are well developed in Brazil (Barbosa et al., 2003;Kageyama et al., 2003), the importance of frugivory for the prac-tical implementation of such programs has only been consideredon theoretical basis (Silva, 2003; Rodrigues and Gandolfi, 2000).The New World fruit-eating bats (Chiroptera: Phyllostomidae) aregoodmodels for such studies.Within Neotropical bats assemblages,fruit-eating species constitute the dominant andmost diverse guildin terms of feeding habits (Kalko, 1998; Medellin et al., 2000;

Dumont, 2003; Giannini and Kalko, 2004; Mello, 2009). Throughseed dispersal, fruit-eating phyllostomid bats play a crucial role themaintenance of tropical ecosystem dynamics (Fleming andHeithaus, 1981; Medellin et al., 2000; Bernard and Fenton, 2007;Henry et al., 2007; Medellin and Gaona, 1999; Galindo-Gonzálezet al., 2000; Arteaga et al., 2006; Henry and Jouard, 2007).Indeed, methods for attracting fruit-eating bats to degraded areasare currently being considered as a mechanism for their effectiverestoration (Bianconi et al., 2007; Kelm et al., 2008).

In this paper we analyse the potential contribution of fruit-eating phyllostomid bats to the input of allochthonous seeds ina restored area in Southeast Brazil. We address two basic questions:a) what are the diets of the fruit-eating bat species already resident

Fig. 1. Localization and general characterization of the RPPN São Marcelo in São Paulo State, Brazil.


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)


(July 2007 and August 2008). We marked twelve individuals ofeach species, and the number of sampled individuals was approx-imately balanced between seasons (see Table 1 for detailed infor-mation). For each monitored individual we followed a samplingprotocol in order to standardize sampling regime over time: eachsampling night was sub-divided into four 3-h intervals, startingat 18 h and ending at 06 h of the next day; during each interval,the entire study area was covered using a vehicle to search formarked individuals. Each individual was monitored for all fourintervals and flight routes and range areas were obtained throughmapping of successive locations and roost fixes. The procedure of

standardizing sampling regime over time allows inference regard-ing habitat use in situations where the number of location fixes dif-fers among individuals (replicates) (Börger et al., 2006). Usually,two or three individuals were simultaneously monitored everynight, and sampling always alternated among all individuals dur-ing each interval. Within the constraints imposed by the batterylife-time, we were able to monitor each individual in the lengthof time required to sample all four intervals in a balanced way.

We performed active searches for the signal and used triangula-tion techniques to obtain locations (Jacob and Rudran, 2003) usinga radio-receiver model TR-5 (Telonics Inc.) coupled to a two-

Fig. 1. Maps of the study area, highlighting Parque São Marcelo and its insertion in the surrounding landscape (MSC). We depict in the maps examples of foraging areas(contours estimated by 95% fixed kernel method) and day roosts (points) of (A) three Carollia perspicillata individuals and (B) three Artibeus lituratus individuals. Each colorrepresents a different individual (replicate).

Table 1Summary 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 Areahabitat; 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 perspicillata1 Female Dry 4 58 0 29.63 46.27 –2 Male Dry 5 31 1 16.33 29.84 722.23 Male Wet 3 6 0 – – –4 Male Wet 4 23 2 15.38 23 495.95 Male Wet 4 25 1 54.43 14.29 617.66 Female Wet 7 21 2 17.47 38.2 1987 Male Wet 5 16 2 23.84 29.45 2628 Female Wet 6 19 1 26.85 49.61 357.79 Female Wet 7 17 2 45.107 25.38 299.1

10 Female Dry 8 27 1 40.17 28.33 958.711 Female Dry 4 17 0 79.15 37.8 –12 Female Dry 4 25 0 28.74 34.02 –Mean ± SD 34.2 ± 19.4 32.3 ± 10.2 488.9 ± 262.1

Artibeus lituratus1 Female Dry 6 17 4 73.64 17.98 788.12 Female Wet 4 18 1 30.01 45.53 2053.23 Female Wet 8 16 0 154.16 41.92 –4 Male Wet 5 27 2 57.35 44.11 20015 Male Wet 3 15 0 6.7 – –6 Male Wet 5 15 1 136.03 23.26 1295.67 Male Wet 6 9 0 – – –8 Male Wet 3 17 0 172.18 35.77 –9 Female Wet 5 25 1 389.72 29.06 1076.2

10 Male Dry 6 15 1 77.94 20.63 650.911 Male Dry 8 20 1 61.53 30.88 98712 Male Dry 4 24 2 90.1 26.45 418.2Mean ± SD 124.3 ± 103.8 31.56 ± 9.9 1158.8 ± 598.6

138 L.C. Trevelin et al. / Forest Ecology and Management 291 (2013) 136–143


(C. perspicillata: Wilks k = 0.0039; d.f. 4; p < 0.001, randomizationp = 0.004; and A. lituratus: Wilks k = 0.0587; d.f. 4; p < 0.001). Thesame patterns emerged when we used habitat availability basedon specifics 100%MPCs in the analyses (C. perspicillata: Wilksk = 0.0769; d.f. 4; p < 0.001, randomization p = 0.004; and A. litura-tus: Wilks k = 0.0805; d.f. 4; p < 0.001).

For both species, observed patterns also remained similar be-tween analysis when comparing specific habitats through pairwisecomparisons, and we ranked habitat preferences based on100%MPCs compositional analysis. Carollia perspicillata showed asignificant preference for Restored areas, also using Secondary forestremnants and Exotic forest plantations more often than expected,although use was not significantly different between the lattertwo habitat types. Together, these three habitats represented84.75 % of the used habitats. Early successional forest and Anthropo-genic land use were less frequently used than expected based ontheir availability on the landscape, accounting for only 15.25% ofuse (Fig. 2 and Table SM1).

For A. lituratus, the Restored areas were also used significantlymore frequently than any other habitat. There was, however, aninversion in the order of use of the following habitats, with Exoticforest plantations more significantly used than Secondary forest rem-nants. In fact, in this case, Secondary forest remnants was used in thesame frequency than expected by its availability on the landscape,differing from the results obtained for C. perspicillata (Fig. 2). Theother habitats, Early successional forest and Anthropogenic landuse, were used significantly less frequently than expected basedon their availability. They were also significantly less used thanExotic forests and Secondary forests. (Fig. 2 and Table SM2).

3.2. Roosting

The use of habitat for day roosting by both species was directedtowards two specific habitats: Secondary forest remnants and Re-stored areas. In fact, we could not found roosts in any of the otherhabitats. Of the 11 day roosts found for eight Carollia perspicillataindividuals, six were found in Secondary forest remnants, while theother five were in Restored areas. Similarly, for Artibeus lituratus, of13 day roosts also found for eight individuals, nine were found inSecondary forest remnants, while the other four were in Restoredareas. When more than one day roost was found for the same indi-vidual of either species, they were always found in the same habitat.In all the locations, bats were found roosting in the foliage of trees.

3.3. Responses to food resource availability

The overall fruit production of plant species that comprise thediets of the bats was continuous, with some species alternating

in peaks of availability. For Solanum mauritianum, there was nofruits available during one month of the wet season (April 2008),whereas Piper aduncum only produced fruits during the month ofFebruary 2008 (wet), differing from the other species analyzed(Fig. 3).

In analyses of % Restored Area Used, neither of the studied spe-cies showed a response to a specific food resource availability; C.perspicillata showed no significant response to the availability ofS. mauritianum (t = 0.09; d.f. 5; p = 0.205) or P. aduncum(t = 1.394; d.f. 9; p = 0.098), and A. lituratus showed no significantresponse to the availability of S. mauritianum (t = 0.457; d.f. 8;p = 0.33) or C. pachystachya (t = 0.984; d.f. 8; p = 0.177). However,with Mean Commuting Distance as a proxy for movement patterns,C. perspicillata presented a significant reduction in response to theavailability of P. aduncum (t = !2.293; d.f. 6; p = 0.031; Fig. 4), apattern not observed in relation to fruit production of S. mauritia-num (t = 4.04; d.f. 6; p = 0.997). Artibeus lituratus still showed no re-sponse to fruit production of S. mauritianum (t = !0.069; d.f. 6;p = 0.474) or C. pachystachya (t = 2.216; d.f. 6; p = 0.96).

4. Discussion

The success of restoring degraded lands depends, to a large ex-tent, on how these habitats manage to recover faunal populations(Bowen et al., 2007). The present study provides evidence that sug-gests a potential recovery by populations of two frugivorous batspecies in a restored area in southeastern Brazil. We found a con-sistent pattern toward the use of forest-structured habitats by bothspecies, revealing the use of restored forests as main foraging androosting habitat for individuals of A. liturarus and C. perspicillata.Although bats were not restricted to them, these habitats weremore frequently used than predicted by their availability, along-side with the other forest-structured habitats available in the land-scape. The positive selection of specific habitats to forage and restimplied by our results shed light on the relative value these habi-tats have for the bats (Palminteri and Peres, 2012) and, conse-quently, to the whole recolonization process.

Both species strictly used forested habitats for day roosting,mainly using the foliage of trees located in Secondary forest rem-nants and, in some cases, in the Restored areas. Several studiesshow that roost availability is a occurrence-limiting resource inthe landscape for bats (Kunz, 1982; Aguirre et al., 2003), and ourfindings corroborate this since both species were very specific inhabitat requirements for roosting. Furthermore, our data suggestthat forest remnants (mostly riparian forests) act as a source ofnew colonist species and individuals (Turner and Corlett, 1996;Lindenmayer et al., 2008), assisting the gradual recolonization ofrestored areas. A similar pattern of habitat selection was observed

Fig. 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 thelandscape used by each species (accessed with 100%MCP – see text for description).

140 L.C. Trevelin et al. / Forest Ecology and Management 291 (2013) 136–143

✓ Testes de Randomização – uso do espaço em % diferente á disponível ✓ Área restaurada – maior % de uso e maior % probabilidade de uso


in foraging movements, with Restored areas being the most fre-quently used foraging habitat for both species. Both these aspectsof our data represent evidence that the restored forest habitat iscontributing to the persistence of A. lituratus and C. perspicillatapopulations in the landscape and extending their distribution.However, determining whether these habitats act as sources orsinks, requires long-term demographic studies (Bowen et al.,2007; Lindell, 2008).

In addition, the Exotic forests habitat was also intensely usedduring movements. Primarily composed of commercial Eucalyptusplantations, this habitat was used in the same proportion as Sec-ondary forest remnants by Artibeus lituratus. Some studies on Neo-tropical bat assemblages have shown recolonization asdependent on the nature of matrix selectivity (Cosson et al.,1999; Albrecht et al., 2007; Meyer and Kalko, 2008), and few eval-uate the importance of these forest plantations and other structur-ally similar land covers as habitat for bats (see Faria et al., 2006;Barlow et al., 2007; and also Borkin and Parsons, 2010, 2011 forstudies in New Zealand). Compared to other anthropogenic landcovers, our data confirms that these forests plantations are usedat least for movements by these bats, suggesting they may enhanceconnectivity in the landscape and facilitate recolonization of newly

restored forests, as long as associated to source habitats(Brockerhoff et al., 2008). Further studies are needed to confirmthese observations.

4.1. Responses to the availability of food resources

Our roosting behavior data supports our hypothesis that theavailability of fruit is determinant in the use of restored forestsby C. perspicillata. They reduced commuting distance by roostingcloser to their feeding area (restored areas) as response to theavailability of Piper aduncun’s infructescenses in this habitat(Fig. 4). Other studies have demonstrated similar behavior and sug-gest that Carollia actively selects Piper species whilst foraging(Fleming and Heithaus, 1986; Thies and Kalko, 2004; Bianconiet al., 2012).

On the other hand, we failed to support other predictions re-lated to direct responses in the use of restored areas, for roostingby A. lituratus and for foraging by both species, to the availabilityof each specific food item in these habitats. This non-direct rela-tionship between the availability of specific food items and forag-ing movement in restored areas could indicate that they may beresponding to food availability in other habitats of the landscape.While this is a valid alternative explanation, we have confirmedthat Restored areas are being used as their main foraging area (thisstudy and Silveira et al., 2011). Considering that overall availabilityof food resource was relatively constant (fruiting plant speciesalternated but maintained overall production; Fig. 3), it is feasibleto assume that constant use of the restored area for foraging re-flects this constancy in overall food availability. Studies in severallocations have shown feeding plasticity for both species (Galettiand Morellato, 1994; Passos et al., 2003; Mello et al., 2004; Silveiraet al., 2011), despite of the purported ‘‘preferences’’ known tophyllostomid (Mello et al., 2011). Our results may demonstratehow this plasticity reflects on foraging behavior (Fleming and Heit-haus, 1986) and, consequently, on the use of the restored areas, aswe initially hypothesized. In a recently restored area, where mostplanted species are not mature enough to bear fruits, these bat spe-cies are adapting their diets to what is available, and, consequently,using space accordingly. From the restoration viewpoint, theseplant species are effective in continuously attracting and retainingthese frugivores, contributing to the initial recovery of the fauna inthis area (Silveira et al., 2011).

4.2. Movement patterns

There is a lack of studies directly estimating home-range orrange areas for A. lituratus, but some studies report movementsover large distances (Morison, 1980; Menezes Jr. et al., 2008) aswell as low fidelity to local forest patches (Bianconi et al., 2006).It is suggested that large Artibeus species have large range areas(Morison, 1978; Handley et al., 1991; Costa et al., 2006) usuallyattributed to feeding preferences for plant species that produceabundant fruit crops over short time periods, generally occurringin low densities over large areas (particularly Moraceae of thegenus Ficus – Handley et al., 1991; Galetti and Morellato, 1994;Passos et al., 2003). In the present study we confirmed the magni-tude expected for range areas (Morison, 1980; Handley et al.,1991), sampled individuals were never restricted to a single patch,and only on a few occasions would they repeat the same pattern ofspace use during sampling days, normally alternating use betweenforest patches present in the landscape. On the other hand, mostindividuals simply flew out of the MSC, indicating that the valueswe presented for range area may be underestimates of the actualrange area of this species.

Carollia perspicillata is a small frugivore whose feeding prefer-ences are concentrated on plant species with low density fruit

Fig. 3. Estimates of fruit availability of the three plant populations identified asmajor items in the diet of both bats species in the study area.

Fig. 4. Box-plot comparing mean commuting distance from roosts to foraging areasfor Carollia perspicillata between periods with and without the presence of ripefruits of Piper aduncum in the population.

L.C. Trevelin et al. / Forest Ecology and Management 291 (2013) 136–143 141

Piper aduncum

1)  Florestais Secundárias AL – 9 abrigos CP – 6 abrigos 2) Área Restaurada AL – 4 abrigos CP – 5 abrigos

13 abrigos 11 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

R E S E A R C H A R T I C L E

Use of Fruit Essential Oils to Assist ForestRegeneration by BatsGledson V. Bianconi,1,2,3 Urubatan M. S. Suckow,4 Ariovaldo P. Cruz-Neto,1

and Sandra B. Mikich5

AbstractFrugivorous bats can be attracted with essential oils fromripe chiropterochoric fruit. We evaluated the efficiency ofthese oils to attract bats in degraded areas within theAtlantic Rain Forest, particularly pasture and agriculturalland. We hypothesized that induction units (IUs), each con-taining a rubber septum impregnated with oil, would havemore bat activity than their respective control units (CUs;without the oil). To test this hypothesis we monitored batflight activity with night-vision infrared visors in eight IUand CU from August 2006 to July 2007. We also verifiedthe probability of arrival of chiropterochoric seeds by ana-lyzing the diet of bats captured in a neighboring forestarea. Our initial hypothesis that units with odor would leadto greater bat activity was confirmed. Results indicated arich community of fruit-eating bats, and dietary analysis

revealed a huge potential for dispersion of a vast amountof seeds from different plant species at the IU. Althoughour study does not reveal with certainty which bat speciesare attracted to the oil, the flying patterns coincide withthose described for the foraging behavior of fruit-eatingphyllostomids. Furthermore, the fact that the bats spendmore time flying around the odor source compared toflying time around CU suggest an increase in seed rain.Taken together, these results suggest that the use of essen-tial oils from chiropterochoric fruits induces a qualitativeand quantitative increase in seed dispersal in areas thatotherwise would not be frequently visited by frugivorousbats.

Key words: Atlantic Forest, bat attraction, conservationbiology, frugivory, fruit-eating bats, fruit odors, restora-tion, seed dispersal.

Introduction

The Brazilian Atlantic Rain Forest is one of the most diverseand threatened biomes in the world (Mittermeier et al. 2005).Remaining areas of Atlantic Forest suffer intense pressuresfrom a variety of anthropogenic activities carried out bya population of more than 120 million people (FundacaoSOS Mata Atlantica/INPE 2008) in the surrounding areas.Today, more than 92% (about 1,200,000 km2) of the originalcontinuous forest landscape (Campanili & Prochnow 2006)is represented by small forest remnants surrounded by anextensive agricultural matrix.

The high level of habitat loss and fragmentation of thisbiome has consequences that extend beyond the loss of biodi-versity. The loss of forest areas also impairs other biologically

1 Departamento de Zoologia, Instituto de Biociencias, UNESP, CP 199, 13506-900Rio Claro, SP, Brazil2 Neotropical Institute: Research and Conservation, CP 19009, 81531-980 Curitiba,PR, Brazil3 Address correspondence to G. V. Bianconi, email [email protected] Curso de Graduacao em Ciencias Biologicas, PUCPR, Rua Imaculada Conceicao1155, 80215-901 Curitiba, PR, Brazil5 Laboratorio de Ecologia, Embrapa Florestas, CP 319, 83411-970 Colombo,PR, Brazil

© 2010 Society for Ecological Restoration Internationaldoi: 10.1111/j.1526-100X.2010.00751.x

and socially relevant aspects such as soil quality, the avail-ability and quality of water, and even the use of inappropriateareas for agriculture and/or areas otherwise protected by law(e.g. Braga et al. 2002; Young & Lustosa 2003). These con-cerns have prompted several researchers to seek strategies torestore the original landscape and to maintain a minimal levelof ecological processes to assure the continued functioning ofthe fragmented landscape (e.g. Bianconi et al. 2007; Tres et al.2007; Viani et al. 2007; Kelm et al. 2008).

The success of any restoration process depends, to a largeextent, on the recruitment of new individuals and plant speciesfrom the seed bank and, perhaps more importantly, the seedrain from dispersers (Jordano 2000; Gandolfi et al. 2007). Infact, seed dispersal forms the foundation for the regenerationof degraded areas, so that processes that negatively affectthe mechanisms of seed dispersal limit the success of therestoration process (Aide & Cavelier 1994; Uhl 1997; Galindo-Gonzalez et al. 2000). For example, when the input ofseeds is too small, any single factor (i.e. predation rate,competition with the already established vegetation, adverseclimate, and soil types) can compromise the germination ofseeds or seedling establishment (Uhl 1997; Gandolfi et al.2007). Thus, the process of restoration will benefit fromany mechanism that maximizes seed dispersal into degradedareas.

Restoration Ecology 1

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

morcegos e áreas restauradas: uma via de mão dupla · morcegos e áreas restauradas: uma via de...

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