Abstract
Euglossine fauna of a large remnant of Brazilian Atlantic forest in eastern Brazil (Reserva Natural Vale) was assessed along an edge-forest gradient towards the interior of the fragment. To test the hypotheses that the structure of assemblages of orchid bees varies along this gradient, the following predictions were evaluated: (i) species richness is positively related to distance from the forest edge, (ii) species diversity is positively related to distance from the edge, (iii) the relative abundance of species associated with forest edge and/or open areas is inversely related to the distance from edge, and (iv) relative abundance of forest-related species is positively related to distance from the edge. A total of 2264 bees of 25 species was assessed at five distances from the edge: 0 m (the edge itself), 100 m, 500 m, 1000 m and 1500 m. Data suggested the existence of an edge-interior gradient for euglossine bees regarding species diversity and composition (considering the relative abundance of edge and forest-related species as a proxy for species composition) but not species richness.
Similar content being viewed by others
References
Aguiar WM, Gaglianone MC (2008) Comunidade de abelhas Euglossina (Hymenoptera: Apidae) em remanescentes de mata estacional semidecidual sobre tabuleiro no estado do Rio de Janeiro. Neotrop Entomol 37:118–125
Aguiar WM, Gaglianone MC (2012) Euglossine bee communities in small forest fragments of the Atlantic Forest, Rio de Janeiro state, southeastern Brazil (Hymenoptera, Apidae). Rev Bras Entomol 56:210–219
Aizen MA, Feinsinger P (1994) Habitat fragmentation, native insect pollinators, and feral honey bees in Argentine “Chaco Serrano”. Ecol Appl 4:378–392
Amorim HB (1984) Florestas nativas dos estados do Rio de Janeiro e Espírito Santo. Inventário Florestal Nacional. Instituto Brasileiro do Desenvolvimento Florestal-IBDF, Brasilia, 204 p
Armbruster WS (1993) Within-habitat heterogeneity in baiting samples of male euglossine bees: possible causes and implications. Biotropica 25:122–128
Batáry P, Holzschuh A, Orci KM, Samu F, Tscharntke T (2012) Responses of plant, insect and spider biodiversity to local and landscape scale management intensity in cereal crops and grasslands. Agric Ecosyst Environ 146:130–136
Becker P, Moure JS, Peralta FJA (1991) More about euglossine bees in Amazonian Forest fragments. Biotropica 23:586–591
Bonilla-Gómez MA (1999) Caracterização da estrutura espaço-temporal da comunidade de abelhas Euglossinas (Hymenoptera, Apidae) na Hiléia Baiana. PhD. Thesis, Universidade Estadual de Campinas, Brasil, xii+153 p
Bowers MA, Dooley JL (1999) A controlled, hierarchical study of habitat fragmentation: responses at the individual, patch, and landscape scale. Landsc Ecol 14:381–389
Cameron SA (2004) Phylogeny and biology of neotropical orchid bees (Euglossini). Annu Rev Entomol 49:377–404
Campos RC, Hernández MIM (2013) Dung beetle assemblages (Coleoptera, Scarabaeinae) in Atlantic forest fragments in southern Brazil. Rev Bras Entomol 57:47–54
Coudrain V, Herzog F, Entling MH (2013) Effects of habitat fragmentation on abundance, larval food and parasitism of a spider-hunting wasp. PLoS One 8:e59286
Didham RK (1997) The influence of edge effects and forest fragmentation on leaf-litter invertebrates in central Amazonia. In: Laurance WF, Bierregaard RO (eds) Tropical forest remnants: ecology, management, and conservation of fragmented communities. University of Chicago Press, Chicago 632p
Didham RK, Ghazoul J, Stork NE, Davis AJ (1996) Insects in fragmented forests: a functional approach. Trends Ecol Evol 11:255–260
Dodson CH, Dressler RL, Hills HG, Williams NH (1969) Biologically active compounds in orchid fragrances. Science 164:1243–1249
Dressler RL (1982) Biology of the orchid bees (Euglossini). Annu Rev Ecol Syst 13:373–394
Ewers RM, Didham RK (2006) Confounding factors in the detection of species responses to habitat fragmentation. Biol Rev 81:117–142
Faria LRR, Melo GAR (2007) Species of Euglossa (Glossura) in the Brazilian Atlantic forest, with taxonomic notes on Euglossa stellfeldi Moure (Hymenoptera, Apidae, Euglossina). Rev Bras Entomol 51:275–284
Faria LRR, Melo GAR (2012) Species of Euglossa of the analis group in the Atlantic forest (Hymenoptera, Apidae). Zoologia 29:349–374
Faria LRR, Sydney NV, Gonçalves, R. B. (2015) How Brazilian researchers have been sampling orchid bees? In: Aguiar AJC, Gonçalves RBG, Ramos KS (org.) Ensaios sobre as abelhas da região Neotropical: homenagem aos 80 anos de Danuncia Urban. Curitiba, Editora UFPR, 456p
Fletcher RJ Jr, Ries L, Battin J, Chalfoun AD (2007) The role of habitat area and edge in fragmented landscapes: definitively distinct or inevitably intertwined? Can J Zool 85:1017–1030
Gerlach J, Samways M, Pryke J (2013) Terrestrial invertebrates as bioindicators: an overview of available taxonomic groups. J Insect Conserv 17:831–850
Gómez JM, Perfectti F, Klingenberg CP (2014) The role of pollinator diversity in the evolution of corolla-shape integration in a pollination-generalist plant clade. Philos Trans R Soc B 369:20130257
Guimarães CDC, Viana JPR, Cornelissen T (2014) A meta-analysis of the effects of fragmentation on herbivorous insects. Environ Entomol 43:537–545
Hamilton AJ (2005) Species diversity or biodiversity? J Environ Manag 75:89–92
Hammer O, Harper DAT, Ryan PD (2001) PAST: paleontological statistics software package for education and data analysis. Palaeontol Electron 4:1–9
Hijmans RJ, Guarino L, Cruz M, Rojas E (2001) Computer tools for spatial analysis of plant genetic resources data: 1. DIVA-GIS. Plant Genet Resour Newsl 127:15–19
Hurlbert SH (1971) The non-concept of species diversity: a critique and alternative parameters. Ecology 52:577–589
Hurlbert SH (1984) Pseudoreplication and the design of ecological field experiments. Ecol Monogr 54:187–211
Janzen DH (1971) Euglossine bees as long-distance pollinators of tropical plants. Science 171:203–205
Jarque C, Bera A (1980) Efficient tests for normality, homoscedasticity and serial independence of regression residuals. Econ Lett 6:255–259
Kark S (2013) Ecotones and ecological gradientes. In: Leemans R (ed) Ecological systems: selected entries from the Encyclopedia of Sustainability Science and Technology. Springer, New York 303p
Knoll FRN, Penatti NC (2012) Habitat fragmentation effects on the orchid bee communities in remnant forests of southeastern Brazil. Neotrop Entomol 41:355–365
Lopes JC, de Mello-Silva R (2014) Annonaceae da Reserva Natural Vale, Linhares, Espírito Santo. Rodriguésia 65:599–635
Mattozo VC, Faria LRR, Melo GAR (2011) Orchid bees (Hymenoptera: Apidae) in the coastal forests of southern Brazil: diversity, efficiency of sampling methods and comparison with other Atlantic forest surveys. Pap Avulsos Zool 51:505–515
Meffe GK, Carroll CR (1997) Principles of conservation biology. Sinauer Associates, Sunderland 779p
Milet-Pinheiro P, Schlindwein C (2005) Do euglossine males (Apidae, Euglossini) leave tropical rainforest to collect fragrances in sugarcane monocultures? Rev Bras Zool 22:853–858
Morato EF (1994) Abundância e riqueza de machos de Euglossini (Hymenoptera: Apidae) em mata de terra firme e áreas de derrubada, nas vizinhanças de Manaus (Brasil). Bol Mus Para Emilio Goeldi, Zool 10:95–105
Moure JS, Melo GAR, Faria LRR (2012) Euglossini Latreille, 1802. In Moure JS, Urban D, Melo GAR (eds) Catalogue of bees (Hymenoptera, Apoidea) in the Neotropical region - online version. http://www.moure.cria.org.br/catalogue. Accessed 10 Feb 2014
Murcia C (1995) Edge effects in fragmented forests: implications for conservation. Trends Ecol Evol 10:58–62
Nemésio A (2009) Orchid bees (Hymenoptera: Apidae) of the Brazilian Atlantic Forest. Zootaxa 2041:1–242
Nemésio A (2011) Euglossa marianae sp. n. (Hymenoptera: Apidae): a new orchid bee from the Brazilian Atlantic Forest and the possible first documented local extinction of a forest-dependent orchid bee. Zootaxa 2892:59–68
Nemésio A (2012) Methodological concerns and challenges in ecological studies with orchid bees (Hymenoptera: Apidae: Euglossina). Biosci J 28:118–135
Nemésio A (2013a) Are orchid bees at risk? First comparative survey suggests declining populations of forestdependent species. Braz J Biol 73:367–374
Nemésio A (2013b) The orchid-bee faunas (Hymenoptera: Apidae) of two Atlantic Forest remnants in southern Bahia, eastern Brazil. Braz J Biol 73:375–381
Nemésio A, Ferrari RR (2012) The species of Eulaema (Eulaema) Lepeletier, 1841 (Hymenoptera: Apidae: Euglossina) from eastern Brazil, with description of Eulaema quadragintanovem sp. n. from the state of Ceará. Zootaxa 3478:123–132
Nemésio A, Rasmussen C (2011) Nomenclatural issues in the orchid bees (Hymenoptera: Apidae: Euglossina) and an updated catalogue. Zootaxa 3006:1–42
Nemésio A, Silveira FA (2006) Edge effects on the orchid-bee fauna (Hymenoptera: Apidae) at a large remnant of Atlantic Forest in southeastern Brazil. Neotrop Entomol 35:313–323
Nemésio A, Silveira FA (2010) Forest fragments with larger core areas better sustain diverse orchid bee faunas (Hymenoptera: Apidae: Euglossina). Neotrop Entomol 39:555–561
Nemésio A, Vasconcelos HL (2014) Effectiveness of two sampling protocols to survey orchid bees (Hymenoptera: Apidae) in the Neotropics. J Insect Conserv 18:197–202
Oliveira MA, Grillo AS, Tabarelli M (2004) Forest edge in the Brazilian Atlantic forest: drastic changes in tree species assemblages. Oryx 38:389–394
Olson DM, Dinerstein E (2002) The Global 200: priority ecoregions for global conservation. Ann Mo Bot Gard 89:199–224
Peixoto AL, Silva IM, Pereira OJ, Simonelli M, Jesus RM, Rolim SG (2008) Tabuleiro forests north of the Rio Doce Natural Reserve, Espírito Santo, Brazil. In: Thomas WW, Britton EG (eds) The Atlantic coastal forest of Northeastern Brazil. The New York Botanical Garden Press, New York 586p
Pinheiro J, Bates D, DebRoy S, Sarkar D (2015) nlme. R package version 3.1–119. https://cran.rproject.org/web/packages/nlme/index.html. Accessed 20 Jan 2015
Prevedello JA, Figueiredo MSL, Grelle CEV, Vieira MV (2013) Rethinking edge effects: the unaccounted role of geometric constraints. Ecography 36:287–299
R Development Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna http://www.R-project.org . Accessed 10 Jun 2015
Ramalho AV, Gaglianone MC, de Oliveira ML (2009) Comunidades de abelhas Euglossina (Hymenoptera, Apidae) em Fragmentos de Mata Atlântica no sudeste do Brasil. Rev Bras Entomol 53:95–101
Ramalho M, Rosa JF, e Silva MD, Silva M, Monteiro D (2013) Spatial distribution of orchid bees in a rainforest/rubber agro-forest mosaic: habitat use or connectivity. Apidologie 44:385–403
Rebêlo JMM, Moure JS (1996) [1995] As espécies de Euglossa Latreille do nordeste de São Paulo (Apidae, Euglossinae). Rev Bras Zool 12:445–466
Resende HC, Yotoko KSC, Delabie JHC, Costa MA, Campiolo S, Tavares MG, Campos LAO, Fernandes-Salomão TM (2010) Pliocene and Pleistocene events shaping the genetic diversity within the central corridor of the Brazilian Atlantic Forest. Biol J Linn Soc 101:949–960
Ribeiro MC, Metzger JP, Martensen AC, Ponzoni FJ, Hirota MM (2009) The Brazilian Atlantic Forest: how much is left, and how is the remaining forest distributed? Implications for conservation. Biol Conserv 142:1141–1153
Ries L, Sisk TD (2010) What is an edge species? The implications of sensitivity to habitat edges. Oikos 119:1636–1642
Scheipl F, Bolker B (2015) RLRsim. R package version 3.1–2. https://cran.rproject.org/web/packages/RLRsim/index.html. Accessed 10 Oct 2015
Silva AG (2014) A importância da Reserva Natural Vale para a conservação das florestas tropicais nativas do Norte do Espírito Santo, Brasil. Natureza Online 12:206–211
Spector S, Ayzama S (2003) Rapid turnover and edge effects in dung beetles assemblages (Scarabaeidae) at a Bolivian Neotropical forest-savanna ecotone. Biotropica 35:394–404
Sydney NV, Gonçalves RB (2015) Is the capture success of orchid bees (Hymenoptera, Apoidea) influenced by different baited trap designs? A case study from southern Brazil. Rev Bras Entomol 59:34–38
Tonhasca A, Blackmer JL, Albuquerque GS (2002) Abundance and diversity of euglossine bees in the fragmented landscape of the Brazilian Atlantic Forest. Biotropica 34:416–422
Tonhasca A, Albuquerque GS, Blackmer JL (2003) Dispersal of euglossine bees between fragments of the Brazilian Atlantic Forest. J Trop Ecol 19:99–102
Valladares G, Salvo A, Cagnolo L (2006) Habitat fragmentation effects on trophic processes on insect-plant food webs. Conserv Biol 20:12–217
Veloso HP, Rangel ALR, Lima JCA (1991) Classificação da vegetação brasileira, adaptada a um sistema universal. IBGE-DERMA, Rio de Janeiro
Acknowledgments
We express our gratitude to Maria Cecília Martins Kierulff for being so helpful and giving us all the support within her reach during the fieldwork at Reserva Natural Vale. We also acknowledge Vale and Reserva Natural Vale administration for allowing us to sample the orchid bees of the preserve under their responsibility and for all the facilities provided during the fieldwork. We are indebted to Arianny Storari, Débora Ferreira, Frederico F. Salles, and Marcos C. Teixeira for all their help with fieldwork. Antonio Carlos “Toninho” Cosme is acknowledged for all the support on logistic issues. Gabriel A. R. Melo (UFPR) is acknowledged for Ex. salsai determination. Karina F. Póvoa and Marcio S. Ferreira, who provided the shapefile of RNV, and Samuel F. Adami (UNILA), who helped us when dealing with this kind of archive, are acknowledged. We thank SISBIO/ ICMBio for the provided collecting permit (#21803) and CEUNES/UFES for providing transport during some field trips.
Author information
Authors and Affiliations
Corresponding author
Additional information
Edited by Fernando B Noll – UNESP
Rights and permissions
About this article
Cite this article
Coswosk, J.A., Ferreira, R.A., Soares, E.D.G. et al. Responses of Euglossine Bees (Hymenoptera, Apidae, Euglossina) to an Edge-Forest Gradient in a Large Tabuleiro Forest Remnant in Eastern Brazil. Neotrop Entomol 47, 447–456 (2018). https://doi.org/10.1007/s13744-017-0533-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13744-017-0533-z