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Monitoring fruit-feeding butterfly assemblages in two vertical strata in seasonal Atlantic Forest: temporal species turnover is lower in the canopy

Published online by Cambridge University Press:  02 November 2017

Jessie Pereira dos Santos*
Affiliation:
Departamento de Biologia Animal, Instituto de Biologia, Universidade Estadual de Campinas, P.O. Box 6109, Campinas, São Paulo 13083-970, Brazil
Cristiano Agra Iserhard
Affiliation:
Departamento de Ecologia, Zoologia e Genética, Instituto de Biologia, Universidade Federal de Pelotas, P.O. Box 354, Pelotas, Rio Grande do Sul 96160-000
Junia Yasmin Oliveira Carreira
Affiliation:
Departamento de Biologia Animal, Instituto de Biologia, Universidade Estadual de Campinas, P.O. Box 6109, Campinas, São Paulo 13083-970, Brazil
André Victor Lucci Freitas
Affiliation:
Departamento de Biologia Animal, Instituto de Biologia, Universidade Estadual de Campinas, P.O. Box 6109, Campinas, São Paulo 13083-970, Brazil
*
*Corresponding author. Email: [email protected].

Abstract:

To address how seasonality affects the richness and abundance of tropical insects, we compared the canopy and understorey communities of fruit-feeding butterflies in a seasonal Atlantic forest in south-eastern Brazil. Butterflies were sampled over 1 y using a standardized design with baited traps. A total of 2047 individuals in 69 species were recorded (1415 in the canopy, 632 in the understorey). Clear differences were found between canopy and understorey, with significantly higher butterfly abundances in the canopy. We observed two marked peaks of abundance and richness in both strata; one at the transition from dry to the wet seasons, and the other at the transition from wet to dry seasons. We found lower species turnover throughout the year in the canopy. We interpret this as evidence that temperature is more important than rainfall in explaining the yearly variation of abundance in vertical strata. The higher temperatures found in the canopy may allow butterflies to maintain activity in this stratum all year round, whereas the understorey is subject to colder temperatures, thus presenting a higher species turnover. These results improve our understanding of diversity gradients between evergreen and seasonal tropical forests, allowing insights into how climate and beta diversity gradients interact.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2017 

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References

LITERATURE CITED

ADUSE-POKU, K., WILLIAM, O., OPPONG, S. K., LARSEN, T., OFORI-BOATENG, C. & MOLLEMAN, F. 2012. Spatial and temporal variation in butterfly biodiversity in a West African forest: lessons for establishing efficient rapid monitoring programmes. African Journal of Ecology 50:326334.CrossRefGoogle Scholar
BASSET, Y., NOVOTNY, V., MILLER, S. E. & KITCHING, R. L. 2003. Arthropods of tropical forests. Spatio-temporal dynamics and resource use in the canopy. Cambridge University Press, Cambridge. 474 pp.Google Scholar
BECCALONI, G. W. 1997. Vertical stratification of ithomiine butterfly (Nymphalidae: Ithomiinae) mimicry complexes: the relationship between adult flight height and larval host plant height. Biological Journal of the Linnean Society 62:313341.Google Scholar
BERNARD, E. 2001. Vertical stratification of bat communities in primary forests of Central Amazon, Brazil. Journal of Tropical Ecology 17:115126.CrossRefGoogle Scholar
BONEBRAKE, T. C., PONISIO, L. C., BOGGS, C. L. & EHRLICH, P. R. 2010. More than just indicators: a review of tropical butterfly ecology and conservation. Biological Conservation 143:18311841.CrossRefGoogle Scholar
BREHM, G. 2007. Contrasting patterns of vertical stratification in two moth families in a Costa Rican lowland rain forest. Basic and Applied Ecology 8: 4454.Google Scholar
BROSE, U. & MARTINEZ, N. D. 2004. Estimating the richness of species with variable mobility. Oikos 105:292300.CrossRefGoogle Scholar
BROWN, K. S. 1991. Conservation of Neotropical environments: insects as indicators. Pp 349–404 in Collins, N. M. & Thomas, J. A. (eds). The conservation of insects and their habitats. Royal Entomological Society Symposium XV, Academic Press, London.Google Scholar
BROWN, K. S. 1992. Borboletas da Serra do Japi: diversidade, habitats, recursos alimentares e variação temporal. Pp. 142–186 in Morellato, L. P. C. (org). História Natural da Serra do Japi: ecologia e preservação de uma área florestal no Sudeste do Brasil. Editora da Unicamp, Campinas.Google Scholar
CHAO, A. & JOST, L. 2012. Coverage-based rarefaction and extrapolation: standardizing samples by completeness rather than size. Ecology 93:25332547.Google Scholar
CHAO, A., GOTELLI, N. J., HSIEH, T. C., SANDER, E., MA, K. H., COLWELL, R. K. & ELLISON, A. M. 2013. Rarefaction and extrapolation with Hill numbers: a framework for sampling and estimation in species diversity studies. Ecological Monographs 84:4567.Google Scholar
CHARLES, E. & BASSET, Y. 2005. Vertical stratification of leaf-beetle assemblages (Coleoptera: Chrysomelidae) in two forest types in Panama. Journal of Tropical Ecology 21:329336.Google Scholar
COLWELL, R. K., CHAO, A., GOTELLI, N. J., LIN, S. Y., MAO, C. X., CHAZDON, R. L. & LONGINO, J. T. 2012. Models and estimators linking individual-based and sample-based rarefaction, extrapolation and comparison of assemblages. Journal of Plant Ecology 5:321.CrossRefGoogle Scholar
DE CÁCERES, M. & LEGENDRE, P. 2009. Associations between species and groups of sites: indices and statistical inference. Ecology 90:35663574.Google Scholar
DEVRIES, P. J. 1987. The butterflies of Costa Rica and their natural history, Volume 1: Papilionidae, Pieridae, Nymphalidae. Princeton University Press, Princeton. 327 pp.Google Scholar
DEVRIES, P. J. 1988. Stratification of fruit-feeding nymphalid butterflies in a Costa Rican forest. Journal of Research on Lepidoptera 26:98108.Google Scholar
DEVRIES, P. J. & WALLA, T. R. 2001. Species diversity and community structure in neotropical fruit-feeding butterflies. Biological Journal of the Linnean Society 74:115.CrossRefGoogle Scholar
DEVRIES, P. J., MURRAY, D. & LANDE, R. 1997. Species diversity in vertical, horizontal, and temporal dimensions of a fruit-feeding nymphalid butterfly community in an Ecuadorian rainforest. Biological Journal of the Linnean Society 62:342364.CrossRefGoogle Scholar
DEVRIES, P. J., WALLA, T. R. & GREENEY, H. F. 1999. Species diversity in spatial and temporal dimensions of fruit-feeding butterfly community in an Ecuadorian rainforest. Biological Journal of the Linnean Society 68:333353.CrossRefGoogle Scholar
DEVRIES, P. J., ALEXANDER, L. G., CHACON, I. A. & FORDYCE, J. A. 2012. Similarity and difference among rainforest fruit-feeding butterfly communities in Central and South America. Journal of Animal Ecology 81:472482.CrossRefGoogle ScholarPubMed
DINGLE, H., ROCHESTER, W. A. & ZALUCKI, M. P. 2000. Relationships among climate, latitude and migration: Australian butterflies are not temperate-zone birds. Oecologia 124:196207.CrossRefGoogle Scholar
DUFRÊNE, M. & LEGENDRE, P. 1997. Species assemblages and indicator species: the need for a flexible asymmetrical approach. Ecological Monographs 67:345366.Google Scholar
DUMBRELL, A. J. & HILL, J. K. 2005. Impacts of selective logging on canopy and ground assemblages of tropical forest butterflies: implications for sampling. Biological Conservation 125:123131.CrossRefGoogle Scholar
FERMON, H., WALTERT, M. & MÜHLENBERG, M. 2003. Movement and vertical stratification of fruit-feeding butterflies in a managed West African rainforest. Journal of Insect Conservation 7:719.Google Scholar
FERMON, H., WALTERT, M., VANE-WRIGHT, R. I. & MÜHLENBERG, M. 2005. Forest use and vertical stratification in fruit-feeding butterflies of Sulawesi, Indonesia: impacts for conservation. Biodiversity and Conservation 14:333350.Google Scholar
FORDYCE, J. A. & DEVRIES, P. J. 2016. A tale of two communities: Neotropical butterfly assemblages show higher beta diversity in the canopy compared to the understory. Oecologia 181:235243.Google Scholar
FREITAS, A. V. L., ISERHARD, C. A., SANTOS, J. P., CARREIRA, J. Y. O., RIBEIRO, D. B., MELO, D. H. A., ROSA, A. H. B., MARINI-FILHO, O. J., ACCACIO, G. M. & UEHARA-PRADO, M. 2014. Studies with butterfly bait traps: an overview. Revista Colombiana de Entomologia 40:209218.Google Scholar
JOST, L. 2006. Entropy and diversity. Oikos 113:363375.CrossRefGoogle Scholar
JOST, L. 2007. Partitioning diversity into independent alpha and beta components. Ecology 88:24272439.CrossRefGoogle ScholarPubMed
JOST, L., CHAO, A. & CHAZDON, R. L. 2011. Compositional similarity and β (beta) diversity. Pp. 66–84 in Magurran, A. E. & McGill, B. J. (eds). Biological diversity: frontiers in measurement and assessment. Oxford University Press, Oxford.Google Scholar
KISHIMOTO-YAMADA, K. & ITIOKA, T. 2015. How much have we learned about seasonality in tropical insect abundance since Wolda (1988)? Entomological Science 18:407419.Google Scholar
MCKEY, D. 1991. Interactions between ants and plants: comparison of canopy, understory and clearing environments. Pp. 66–73 in Hallé, F. & Pascal, O. (eds). Biologie d'une canopée de forêt équatoriale. Longman, Paris.Google Scholar
MOLLEMAN, F., ARJAN, K., BRAKEFIELD, P. M., DEVRIES, P. J. & ZWAAN, B. J. 2006. Vertical and temporal patterns of biodiversity of fruit-feeding butterflies in a tropical forest in Uganda. Biodiversity and Conservation 15:107121.CrossRefGoogle Scholar
MORELLATO, L. P. C. 1992a. Sazonalidade e dinâmica de ecossistemas florestais na Serra do Japi. Pp. 98110 in Morellato, L. P. C. (ed.). História Natural da Serra do Japi: ecologia e preservação de uma área florestal no Sudeste do Brasil. Editora da Unicamp, Campinas.Google Scholar
MORELLATO, L. P. C. 1992b. Nutrient cycling in two southeast Brazilian forests. I Litterfall and litter standing crop. Journal of Tropical Ecology 8:205215.Google Scholar
MORELLATO, L. P. C. & LEITÃO-FILHO, H. F. 1992. Padrões de frutificação e dispersão na Serra do Japi. Pp. 112140 in Morellato, L. P. C. (ed.). História Natural da Serra do Japi: ecologia e preservação de uma área florestal no Sudeste do Brasil. Editora da Unicamp, Campinas.Google Scholar
MORELLATO, L. P. C. & HADDAD, C. F. B. 2000. Introduction: the Brazilian Atlantic Forest. Biotropica 32:786792.Google Scholar
MORELLATO, L. P. C., TALORA, D. C., TAKAHASHI, A., BENCKE, C. S. C., ROMERA, E. C. & ZIPARRO, V. 2000. Phenology of Atlantic rain forest trees: a comparative study. Biotropica 32:811823.Google Scholar
OLIVEIRA-FILHO, A. T. & FONTES, M. A. L. 2000. Patterns of floristic differentiation among Atlantic Forests in southeastern Brazil and the influence of climate. Biotropica 32:793810.Google Scholar
PEARSON, D. L. & CARROLL, S. S. 1998. Global patterns of species richness: spatial models for conservation planning using bioindicator and precipitation data. Conservation Biology 12:809821.Google Scholar
PINTO, H. S. 1992. Clima da Serra do Japi. Pp. 3038 in Morellato, L. P. C. (ed.). História Natural da Serra do Japi: ecologia e preservação de uma área florestal no Sudeste do Brasil. Editora da Unicamp, Campinas.Google Scholar
QUEIROZ, J. M. 2002. Host plant use among closely related Anaea butterfly species (Lepidoptera, Nymphalidae, Charaxinae). Brazilian Journal of Biology 62:657663.Google Scholar
RIBEIRO, D. B. & FREITAS, A. V. L. 2010. Differences in thermal responses in a fragmented landscape: temperature affects the sampling of diurnal, but not nocturnal fruit-feeding Lepidoptera. Journal of Research on Lepidoptera 42:14.Google Scholar
RIBEIRO, D. B. & FREITAS, A. V. L. 2012. The effect of reduced-impact logging on fruit-feeding butterflies in Central Amazon, Brazil. Journal of Insect Conservation 16:733744.CrossRefGoogle Scholar
ROISIN, Y., DEJEAN, A., CORBARA, B., ORIVEL, J., SAMANIEGO, M. & LEPONCE, M. 2006. Vertical stratification of the termite assemblage in a neotropical rainforest. Oecologia 149:301311.CrossRefGoogle Scholar
SANTOS, J. P., MARINI-FILHO, O. J., FREITAS, A. V. L. & UEHARA-PRADO, M. 2016. Monitoramento de borboletas: o papel de um indicador biológico na gestão de unidades de conservação. Biodiversidade Brasileira 6:8799.Google 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 153:133152.Google Scholar
SMITH, A. P. 1973. Stratification of temperate and tropical forests. American Naturalist 107:671683.CrossRefGoogle Scholar
STORK, N. E. & GRIMBACHER, P. S. 2007. Vertical stratification of feeding guilds and body size in beetle assemblages from an Australian tropical rainforest. Austral Ecology 32:7785.Google Scholar
TÓTHMÉRÉSZ, B. 1995. Comparison of different methods for diversity ordering. Journal of Vegetal Science 6:283290.Google Scholar
TREGIDGO, D. J., QIE, L., BARLOW, J., SODHI, N. S. & LIM, S. L. 2010. Vertical stratification responses of an arboreal dung beetle species to tropical forest fragmentation in Malaysia. Biotropica 42:521525.CrossRefGoogle Scholar
TURNER, J. R. G., GATEHOUSE, C. M. & COREY, C. A. 1987. Does solar energy control organic diversity? Butterflies, moths and the British climate. Oikos 48:195205.Google Scholar
UEHARA-PRADO, M., BROWN, K. S. & FREITAS, A. V. L. 2007. Species richness, composition and abundance of fruit-feeding butterflies in the Brazilian Atlantic Forest: comparison between a fragmented and a continuous landscape. Global Ecology and Biogeography 16: 4354.Google Scholar
VIEIRA, E. M. & MONTEIRO-FILHO, E. L. A. 2003. Vertical stratification of small mammals in the Atlantic rain forest of southeastern Brazil. Journal of Tropical Ecology 19:501507.Google Scholar
WALTHER, B. A. 2002. Vertical stratification and use of vegetation and light habitats by Neotropical forest birds. Journal of Ornithology 143:6481.Google Scholar
WEISS, M., PROCHÁZKA, J., SCHLAGHAMERSKÝ, J. & CIZEK, L. 2016. Fine-scale vertical stratification of saproxylic beetles in lowland and montane forests: similar patterns despite low fauna overlap. PLoS ONE 11:118.CrossRefGoogle ScholarPubMed
WOLDA, H. 1988. Insect seasonality: why? Annual Review of Ecology and Systematics 19:118.CrossRefGoogle Scholar
WOOD, B. & GILLMAN, M. P. 1998. The effect of disturbance on forest butterflies using two methods of sampling in Trinidad. Biodiversity and Conservation 7:597616.Google Scholar
XING, S., BONEBRAKE, T. C., TANG, C. C., PICKETT, E. J., CHENG, W., GREENSPAN, S. E., WILLIAMS, S. E. & SCHEFFERS, B. R. 2016. Cool habitats support darker and bigger butterflies in Australian tropical forests. Ecology and Evolution 6:80628074.Google Scholar