Hostname: page-component-78c5997874-94fs2 Total loading time: 0 Render date: 2024-11-10T06:36:36.723Z Has data issue: false hasContentIssue false
  • English
  • Français

Vertical stratification in bat assemblages of the Atlantic Forest of south-eastern Brazil

Published online by Cambridge University Press:  21 September 2017

Renato Gregorin ,
Enrico Bernard ,
Karina Weiser Lobão ,
Luciany Ferreira Oliveira ,
Felipe Santana Machado ,
Bruno Bret Gil  and
Valéria da Cunha Tavares
Renato Gregorin*
Affiliation:
Programa de Pós-Graduação em Ecologia Aplicada, Universidade Federal de Lavras, Lavras, MG.Brazil
Enrico Bernard
Affiliation:
Laboratório de Ciência Aplicada à Conservação da Biodiversidade, Departamento de Zoologia, Universidade Federal de Pernambuco, Recife, PE.Brazil
Karina Weiser Lobão
Affiliation:
Programa de Pós-Graduação em Ecologia Aplicada, Universidade Federal de Lavras, Lavras, MG.Brazil
Luciany Ferreira Oliveira
Affiliation:
Programa de Pós-Graduação em Ecologia Aplicada, Universidade Federal de Lavras, Lavras, MG.Brazil
Felipe Santana Machado
Affiliation:
Programa de Pós-Graduação em Ecologia Aplicada, Universidade Federal de Lavras, Lavras, MG.Brazil
Bruno Bret Gil
Affiliation:
Programa de Pós-Graduação em Ecologia Aplicada, Universidade Federal de Lavras, Lavras, MG.Brazil
Valéria da Cunha Tavares
Affiliation:
Departamento de Zoologia, Universidade Federal de Minas Gerais (UFMG), Belo Horizonte, Minas Gerais MG.Brazil Departamento de Biologia, Universidade Estadual de Minas Gerais (UEMG), Ibirité MG.Brazil
*
*Corresponding author. Email: rgregorin@dbi.ufla.br
Get access Rights & Permissions [Opens in a new window]

Abstract:

Tropical forests are three-dimensional spaces with species and resources heterogeneously distributed. The vertical stratification of tropical forest biotas has been observed for several organisms and regions, but, surprisingly, the vertical structuring of large areas of important tropical forests, such as Brazil's Atlantic Forest, remains poorly studied. Here, we addressed the use of different Atlantic Forest strata by bats, comparing ensemble composition and relative abundance between the understorey and the canopy. A total of 618 bats belonging to 31 species and four families were recorded, including 11 species of frugivores and seven species of gleaning insectivores, the two trophic guilds predominantly represented in our sampling. Fifteen species were captured exclusively in the canopy, and six exclusively in the understorey, and many of those species were represented by a low number of captures (<5). The bat species composition, richness and relative abundance between canopy and understorey strata varied. Chiroderma villosum was exclusively captured in the canopy, Artibeus lituratus was netted predominantly in the canopy and Carollia perspicillata and Desmodus rotundus were mostly captured in the understorey. Although processes such as resource partitioning between species and ecomorphological constraints may explain the differential use of forest strata, this remains little understood because of the scarcity of data for the Atlantic forest canopies.

Keywords

canopy diversityChiropteraMata AtlânticaRio Doce State Park
Type
Research Article
Information
Journal of Tropical Ecology , Volume 33 , Issue 5 , September 2017 , pp. 299 - 308
Copyright
Copyright © Cambridge University Press 2017 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

LITERATURE CITED

ANDERSON, M., GORLEY, R. N. & CLARKE, R. K. 2008. Permanova+ for Primer: guide to software and statistical methods. Plymouth Marine Laboratory, Plymouth, 214 pp.Google Scholar
AYRES, M., AYRES, M. JR., AYRES, D. L. & SANTOS, A.S. 2007. Bioestat 5.0 – aplicações estatísticas nas áreas das ciências biológicas e médicas. Sociedade Civil Mamirauá, Belém. 364 pp.Google Scholar
BARKER, M. G. & PINARD, M. A. 2001. Forest canopy research: sampling problems, and some solutions. Plant Ecology 153:23–38.CrossRefGoogle Scholar
BASSET, Y., CIZEK, L., CUÉNOUD, P., DIDHAM, R. K., GUILHAUMON, F., MISSA, O., ODEGAARD, F., ROSLIN, T., SCHMIDT, J., TISHECHKIN, A. K., WINCHESTER, N. N., ROUBIK, D. W., ABERLENC, H., BAIL, J., BARRIOS, H., BRIDLE, J. R., CASTAÑO-MENESES, G., CORBANA, B., CURLETTI, G., ROCHA, W. D., BAKKER, D., DELABIE, J. H. C., DEJEAN, A., FAGAN, L. L., FLOREN, A., KITCHING, R. L., MEDIANERO, E., MILLER, S. E., OLIVEIRA, E. G., ORIVEL, J., POLLET, M., RAPP, M., RIBEIRO, S. P., ROISIN, Y., SCHMIDT, J. B., SORENSEN, L. & LEPONCE, M. 2012. Arthropod diversity in a tropical forest. Science 338:1481–1484.CrossRefGoogle Scholar
BERGALLO, H. G., ESBÉRARD, C. E. L., MELLO, M. A. R., LINS, V., MONGOLIN, R., MELO, G. G. S. & BAPTISTA, M. 2003. Bat species richness in Atlantic Forest: what is the minimum sampling effort? Biotropica 35:278–288.Google Scholar
BERNARD, E. 2001. Vertical stratification of bat communities in primary forests of central Amazon, Brazil. Journal of Tropical Ecology 17:115–126.CrossRefGoogle Scholar
BOVINI, M. G., CARVALHO-OKANO, R. M. & VIEIRA, M. F. 2001. Malvaceae A. Juss. no Parque Estadual do Rio Doce, Minas Gerais, Brasil. Rodriguésia 52:17–47.CrossRefGoogle Scholar
CARVALHO, F. & FABIÁN, M. H. 2011. Método de elevação de redes de neblina em dosséis florestais para amostragem de morcegos. Chiroptera Neotropical 17:895–902.Google Scholar
CLARKE, K. R. 1993. Non-metric multivariate analyses of changes in community structure. Australian Journal of Ecology 18:117–143.Google Scholar
CONDIT, R., PITMAN, N., LEIGH, E. C. J. R., CHAVE, J., TERBORGH, J., FOSTER, R. B., NÚÑEZ, P., AGUILAR, S., VALENCIA, R., VILLA, G., MULLER-LANDAU, H. C., LOSOS, E. & HUBBELL, S. P. 2002. Beta-diversity in tropical forest trees. Science 295:666– 669.CrossRefGoogle ScholarPubMed
DALPONTE, J. C., GREGORIN, R., ESTEVES-COSTA, V., ROCHA, E. C. & MARCELINO, R. 2016. Bat survey of the lower Juruena River and five new records for the state of Mato Grosso, Brazil. Acta Amazonica 46:227–232.Google Scholar
DIAS, D., PERACCHI, A. L. & SILVA, S. S. P. 2002. Quirópteros do Parque Estadual da Pedra Branca, Rio de Janeiro, Brasil (Mammalia, Chiroptera). Revista Brasileira de Zoologia 19:113–140.Google Scholar
DUFRENE, M., & LEGENDRE, P. 1997. Species assemblages and indicator species: the need for a flexible asymmetrical approach. Ecological Monographs 67:345–366.Google Scholar
ERWIN, T. 1988. The tropical forest canopy: the heart of biotic diversity. Pp. 123–129 in Wilson, E. O. (ed.). Biodiversity. National Academic Press, Washington, DC.Google Scholar
FENTON, B. B., CUMMING, D. H. M., RAUTENBACH, I. L., CUMMING, G. S., CUMMING, M. S., FORD, G. S., TAYLOR, R. D., DUNLOP, J. M., HOVORKA, M. D., JOHNSTON, D. S., PORTFORS, C. V., KALCOUNIS, M. C. & MAHLANGA, Z. 1998. Bats and the loss of tree canopy in African woodland. Conservation Biology 12:339–407.CrossRefGoogle Scholar
GIVNISH, T. J. 1999. On the gradients in tropical trees diversity. Journal of Ecology 87:193–210.CrossRefGoogle Scholar
GREGORIN, R., VASCONCELLOS, K. L. & GIL, B. B. 2015. Two new range records of bats (Chiroptera: Phyllostomidae) for the Atlantic Forest, eastern Brazil. Mammalia 79:121–124.Google Scholar
GREGORIN, R., MORAS, L. M., ACOSTA, L. H., VASCONCELLOS, K. L., POMA, J. L., SANTOS, F. R. & PACA, R. C. 2016. A new species of Eumops (Chiroptera: Molossidae) from southeastern Brazil and Bolivia. Mammalian Biology 81:235–246.Google Scholar
GRELLE, C. E. V. 2003. Forest structure and vertical stratification of small mammals in a secondary Atlantic Forest, southeastern Brazil. Studies on Neotropical Fauna and Environment 38:81–85.CrossRefGoogle Scholar
HANDLEY, C. O. 1967. Bats of the canopy of an Amazonian forest. Atas Simpósio Biota Amazônica 5:211–215.Google Scholar
HENRY, M., BERRIÈRE, P., GAUTIER-HION, A. & COLYN, M. 2004. Species composition, abundance and vertical stratification of a bat community (Megachiroptera: Pteropodidae) in a West African rain forest. Journal of Tropical Ecology 20:21–29.CrossRefGoogle Scholar
HODGKISON, R., BALDING, S. T., ZUBAID, A. & KUNZ, T. H. 2004. Habitat structure, wing morphology, and the vertical stratification of Malaysian fruit bats (Megachiroptera: Pteropodidae). Journal of Tropical Ecology 20:667–673.CrossRefGoogle Scholar
HUMPHREY, P. S., BRIDGE, D. & LOVEJOY, T. E. 1968. A technique for mist-netting in the forest canopy. Bird Banding 39:43–50.CrossRefGoogle Scholar
KALKO, E. K. V. & HANDLEY, C. O. 2001. Neotropical bats in canopy: diversity, community structure, and implications for conservation. Plant Ecology 153:319–333.CrossRefGoogle Scholar
KALKO, E. K. V., HANDLEY, C. O. & HANDLEY, D. 1996. Organization, diversity, and long-term dynamics of a Neotropical bat community. Pp. 503–553 in Cody, M. & Smallwood, J. (eds). Long-term studies in vertebrate communities. Academic Press, Los Angeles.CrossRefGoogle Scholar
KAYS, R. & ALLISON, A. 2001. Arboreal tropical forest vertebrates: current knowledge and research trends. Plant Ecology 153:109–120.Google Scholar
LOPES, W. P., SILVA, A. F., SOUZA, A. L. & NETO, J. A. A. M. 2002. Estrutura fitossocióloga de um trecho de vegetação arbórea no Parque Estadual do Rio Doce - Minas Gerais, Brasil. Acta Botanica Brasilica 16:443–456.Google Scholar
LOWMAN, M. D. & NADKARNI, N. M. 1995. Forest canopies. Academic Press, San Diego. 624 pp.Google Scholar
LOWMAN, M. D. & WITTMAN, P. K. 1996. Forest canopies: methods, hypothesis, and future directions. Annual Review in Ecology and Systematics 27:55–81.Google Scholar
MARINELLO, M. M. & BERNARD, E. 2014. Wing morphology of Neotropical bats: a quantitative and qualitative analysis with implications for habitat use. Canadian Journal of Zoology 92:141–147.CrossRefGoogle Scholar
MARQUES, J. T., PEREIRA, M. J. R. & PALMEIRIM, J. M. 2015. Patterns in the use of rainforest vertical space by Neotropical aerial insectivorous bats: all the action is up in the canopy. Ecography 38:1–11.Google Scholar
MARTINS, M. A., CARVALHO, W. D., DIAS, D., FRANÇA, D. S., OLIVEIRA, M. B. & PERACCHI, A. L. 2015. Bat species richness (Mammalia, Chiroptera) along an elevational gradient in the Atlantic Forest of Southeastern Brazil. Acta Chiropterologica 17:401–409.CrossRefGoogle Scholar
MELO, F. P. L., DIRZO, R. & TABARELLI, M. 2006. Biased seed rain in forest edge: evidence from the Brazilian Atlantic forest. Biological Conservation 132:50–60.Google Scholar
MENDES, G., ARROYO-RODRÍGUEZ, V., ALMEIDA, W. R., PINTO, S. R. R., PILLAR, V. D. & TABARELLI, M. 2016. Plant trait distribution and the spatial reorganization of tree assemblages in a fragmented tropical forest landscape. Plant Ecology 217:31–42.Google Scholar
MEYER, C. F. J., AGUIAR, L. M. S., AGUIRRE, L. F., BAUMGARTEN, J., CLARKE, F. M., COSSON, J. F., VILLEGAS, S. E., FAHR, J., FARIA, D., FUREY, N., HENRY, M., HODGKISON, R., JENKINS, R. K. B., JUNG, K. G., KINGSTON, T., KUNZ, T. H., GONZALEZ, M. C. M., MOYA, I., PONS, J. M., RACEY, P. A., REX, K., SAMPAIO, E. M., STONER, K. E., VOIGT, C., STADEN, D., WEISE, C. D. & KALKO, E. K. V. 2010. Long-term monitoring of tropical bats for anthropogenic impact assessment: gauging the statistical power to detect population change. Biological Conservation 143:7297–2807.CrossRefGoogle Scholar
MEYER, C. F. J., AGUIAR, L. M. S., AGUIRRE, L. F., BAUMGARTEN, J., CLARKE, F. M., COSSON, J. F., VILLEGAS, S. E., FAHR, J., FARIA, D., FUREY, N., HENRY, M., RODGKISON, R., JENKINS, R. K. B., JUNG, K. G., KINGSTON, T., KUNZ, T. H., GONZALEZ, M. C. M., MOYA, I., PATTERSON, B. D., PONS, J. M., RACEY, P. A., REX, K., SAMPAIO, E. M., SOLARI, S., STONER, K. E., VOIGT, C. C., STADEN, D. V., WEISE, C. D. & KALKO, E. K. V. 2011. Accounting for detectability improves estimates of species richness in tropical bat surveys. Journal of Applied Ecology 48:777–787.Google Scholar
NAKAMURA, A., ROGER, L. K., CAO, M., CREEDY, T. J., FAYLE, T. M., FREIBERG, M., HEWITT, C. N., ITIOKA, T., KOH, L. P., MA, K., MALHI, Y., MITCHELL, A., NOVOTNY, V., OZANNE, C. M. P., SONG, L., WANG, H. & ASHTON, L. A. 2017. Forest and their canopies: achievements and horizons in canopy science. Trends in Ecology and Evolution 2233:483–451.Google Scholar
NUNES, S. R. D. F. S., GARCIA, F. C. P., LIMA, H. C. & CARVALHO-OKANO, R. M. 2007. Mimosoideae (Leguminosae) arbóreas do Parque Estadual do Rio Doce, Minas Gerais, Brasil: distribuição geográfica e similaridade florística na Floresta Atlântica no Sudeste do Brasil. Rodriguésia 58:403–421.CrossRefGoogle Scholar
OZANNE, M. P., ANHUF, D., BOULTER, S. L., KELLER, M., KITCHING, R. L., KÖRNER, C., MEINZER, F. C., MITCHELL, A. W., NAKASHIZUKA, T., SILVA DIAS, P. L., STORK, N. E., WRIGHT, S. J. & YOSHIMURA, M. 2003. Biodiversity meets the atmosphere: a global view of forest canopies. Science 301:183–186.Google Scholar
PASSAMANI, M. 1995. Vertical stratification of small mammals in Atlantic hill forest. Mammalia 59:276–279.Google Scholar
PEARSON, D. L. 1971. Vertical stratification of birds in a tropical dry forest. The Condor 73:46–55.CrossRefGoogle Scholar
PENNINGTON, R. T. & DICK, C. W. 2010. Diversification of the Amazonian flora and its relation to key geological and environmental events: a molecular perspective. Pp. 373–385 in Hoorn, C. & Wesselingh, F. P. (eds) Amazonia, landscape and species evolution. Blackwell Publishing, Oxford.Google Scholar
PEREIRA, M. J. R., MARQUES, J. T. & PALMEIRIM, J. M. 2010. Vertical stratification of bat assemblages in flooded and unflooded Amazonian forests. Current Zoology 56:469–478.CrossRefGoogle Scholar
PIRES, D. P. S. & FABIÁN, M. E. 2013. Diversidade, riqueza e estratificação vertical de espécies de morcegos em um remanescente de Mata Atlântica no sul do Brasil. Biotemas 26:121–131.CrossRefGoogle Scholar
REX, K., MICHENER, R., KUNZ, T. H. & VOIGT, C. 2011. Vertical stratification of Neotropical leaf-nosed bats (Chiroptera: Phyllostomidae) revealed by stable isotopes. Journal of Tropical Ecology 27:211–222.Google Scholar
RIBEIRO, M. C., METZGER, J. P., MARTENSEN, A. C., PONZONI, F. J. & HIROTA, M. M. 2009. The Brazilian Atlantic Forest: how much is left, and how is the remaining forest distributed? Implications for conservation. Biological Conservation 142:1141–1153.CrossRefGoogle Scholar
RUSSO, D., CISTRONE, L. & JONES, G. 2007. Emergence time in forest bats: the influence of canopy closure. Acta Oecologica 31:119–126.Google Scholar
SAMPAIO, E. M., KALKO, E. K. V., BERNARD, E., RODRÍGUEZ-HERRERA, B. & HANDLEY, C. O. JR. 2003. A biodiversity assessment of bats (Chiroptera) in a tropical lowland rainforest of central Amazonia, including methodological and conservation considerations. Studies on Neotropical Fauna and Environment 38:17–31.Google Scholar
SANTO-SILVA, E. E., ALMEIDA, W. R., MELO, F. P. & TABARELLI, M. 2013. The nature of seedling assemblages in a fragmented tropical landscape: implications for forest regeneration. Biotropica 45:386–394.CrossRefGoogle Scholar
SANTO-SILVA, E. E., WITHEY, K. D., ALMEIDA, W. R., MENDES, G., LOPES, A. V. & TABARELLI, M. 2015. Seeding assemblages and the alternative successional pathways experienced by Atlantic forest fragments. Plant Ecology and Diversity 8:483–492.CrossRefGoogle Scholar
SCHULZE, C. H., LINSENMAIR, K. E. & FIEDLER, K. 2001. Understorey versus canopy: patterns of vertical stratification and diversity among Lepidoptera in a Bornean rain forest. Plant Ecology 153:133–152.Google Scholar
SEDIO, B. E., WRIGHT, S. J. & DICK, C. W. 2012. Trait evolution and the coexistence of a species swarm in the tropical forest understorey. Journal of Ecology 100:1183–1193.CrossRefGoogle Scholar
SIKES, R. S. & THE ANIMAL CARE AND USE COMMITTEE OF THE AMERICAN SOCIETY OF MAMMALOGISTS. 2016. 2016 guidelines of the American Society of Mammalogists for the use of wild mammals in research and education. Journal of Mammalogy 97:663–688.CrossRefGoogle ScholarPubMed
SIMMONS, N. B. & VOSS, R. S. 1998. The mammals of Paracou, French Guiana: a Neotropical lowland rainforest fauna part I. Bats. Bulletin of the American Museum of Natural History 237:1–219.Google Scholar
STRAUBE, F. C. & BIANCONI, G. V. 2002. Sobre a grandeza e a unidade amostral utilizada para estimar esforço de captura com utilização de redes-de-neblina. Chiroptera Neotropical 8:150–152.Google Scholar
TABARELLI, M., AGUIAR, A. V., GIRÃO, L. C., PERES, C. A. & LOPES, A. V. 2010. Effects of pioneer tree species hyperabundance on forest fragments in northeastern Brazil. Conservation Biology 24:1654–1663.CrossRefGoogle ScholarPubMed
TAVARES, V. C. 2013. Phyllostomid bat wings from Atlantic Forest bat ensembles: an ecomorphological study. Chiroptera Neotropical 19:57–70.Google Scholar
TAVARES, V. C. & ANCIÃES, M. 1998. Artificial roosts and diet of some insectivorous bats in the Parque Estadual do Rio Doce, Brazil. Bat Research News 39:142.Google Scholar
TAVARES, V. C., PERINI, F. A. & LOMBARDI, J. A. 2007. The bat communities (Chiroptera) of the Parque Estadual do Rio Doce, a continuous remnant of Atlantic Forest in southeastern Brazil. Lundiana 8:35–47.Google Scholar
TAVARES, V. C., OLIVEIRA, C. C. N., PALMUTI, C. F. S., NOGUEIRA, E. P. P., GOMES, J. D., MARCOS, M. H., SILVA, R.F., FARIAS, S. & BOBROWIEC, P. E. D. 2017. The bat fauna from Southwestern Brazil, and its affinities with the fauna of western Amazon. Acta Chiropterologica 19:93–106.Google Scholar
VELAZCO, P. M., GREGORIN, R., VOSS, R. S., SIMMONS, N. B. 2014. Extraordinary local diversity of disk-winged bats (Thyropteridae: Thyroptera) in Northern Peru, with the description of a new species and comments on rooting behavior. American Museum Novitates 3795:1–28.CrossRefGoogle Scholar
VIEIRA, E. M. & MONTEIRO-FILHO, E. L. A. 2003. Vertical stratification of small mammals in the Atlantic rain forest of south-eastern Brazil. Journal of Tropical Ecology 19:501–507.CrossRefGoogle Scholar
VOSS, R. S. & EMMONS, L. H. 1996. Mammalian diversity in Neotropical lowland rainforest: a preliminary assessment. Bulletin of the American Museum of Natural History 230:1–115.Google Scholar
VOSS, R. S., LUND, D. P. & SIMMONS, N. B. 2001. The mammals of Paracou, French Guiana: a Neotropical lowland rainforest fauna Part 2. Nonvolant species. Bulletin of the American Museum of Natural History 263:1–1236.2.0.CO;2>CrossRefGoogle Scholar
VOSS, R. S., FLECK, D. W., STRAUSS, R. E., VELAZCO, P. M. & SIMMONS, N. B. 2016. Roosting ecology of Amazonian bats: evidence for guild structure in hyperdiverse mammalian communities. American Museum Novitates 3870:1–43.Google Scholar
WALTHER, B. A. 2002. Vertical stratification and use of vegetation and light habitats by Neotropical forest birds. Journal of Ornithology 143:64–81.Google Scholar
WILLIG, M. R. 1986. Bat community structure in South America: a tenacious chimera. Revista Chilena de Historia Natural 59:151–168.Google Scholar
WRIGHT, S. J. 2002. Plant diversity in tropical forests: a review of mechanisms of species coexistence. Oecologia 130:1–14.Google Scholar
YANG, X., SCHAAF, C., STRAHLER, A., KUNZ, T., FULLER, N., BETKE, M., WU, Z., WANG, Z., THERIAULT, D., CULVENOR, D., JUPP, D. & NEWNHAM, J. L. 2013. Study of bat flight behavior by combining thermal images analysis with LiDAR forest reconstruction. Canadian Journal of Remote Sensing 38:S112–S125.Google Scholar
YANOVIAK, S. P. & KASPARI, M. 2000. Community structure and the habitat templet: ants in the tropical forest canopy and litter. Oikos 89:259–266.Google Scholar