Abstract
Given the decline of pollinators around the world, preserving these animals has become a priority. This is especially urgent in threatened areas that concentrate high biodiversity such as the Atlantic forest (AF) in South America. Orchid bees are among the most important pollinators in the AF and are considered as good biological indicators of environmental quality. However, the populations of these bees have been reduced in size as a result of environmental impacts caused by human activities. In the present study, we used historical climate modelling to infer the refuge areas within the AF that concentrate high genetic diversity of orchid bees. From a total of 235 records of ten species, we built species models for the current days, Mid-Holocene and Last Glacial Maximum periods using MaxEnt program. Our results show refuge areas separately for each species, which may harbor their high levels of individual genetic diversity in the AF. On the other hand, the assemblage-scale model of climate stability shows a large continuous range of suitable areas from the southern to the northern AF, divided into three main stability zones (northeastern, central and southeastern-southern) where putatively are concentrated high levels of genetic diversity for most of these bees. This inference of stability zones should be useful to direct the choice of new conservation units in the AF, mainly in the northern portion of the AF, where the zone of greater suitability for orchid bees analyzed is present, which has been under protected and has experienced an increase of deforestation in the recent years. Finally, we point out that phylogeographic studies with these bees are necessary and might validate our findings.
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References
Anderson RP, Raza A (2010) The effect of the extent of the study region on GIS models of species geographic distributions and estimates of niche evolution: preliminary tests with montane rodents (genus Nephelomys) in Venezuela. J Biogeogr 37:1378–1393. https://doi.org/10.1111/j.1365-2699.2010.02290.x
Basu P, Bhattacharya R, Iannetta PPM (2011) A decline in pollinator dependent vegetable crop productivity in India indicates pollination limitation and consequent agro-economic crises. Nat Preced. hdl:10101/npre.2011.6044.1
Batalha-Filho H, Irestedt M, Fjeldså J, Ericson Per GP, Silveira LF, Miyaki CY (2013) Molecular systematics and evolution of the Synallaxis ruficapilla complex (Aves: Furnariidae) in the Atlantic Forest. Mol Phylogenet Evol 67:86–94
Benedick S, Hill JK, Mustaffa N et al (2006) Impacts of rain forest fragmentation on butterflies in northern Borneo: species richness, turnover and the value of small fragments. J Appl Ecol 43:967–977. https://doi.org/10.1111/j.1365-2664.2006.01209.x
Biesmeijer JC, Roberts SPM, Reemer M, Ohlemüller R, Edwards M, Peeters T, Schaffers AP, Potts SG, Kleukers R, Thomas CD, Settele J, Kunin WE (2006) Parallel Declines in Pollinators and Insect-Pollinated Plants in Britain and the Netherlands. Science 313:351–354. https://doi.org/10.1126/science.1127863
Bodin Ö, Tengö M, Norman A, Lundberg J, Elmqvist T (2006) The value of small size: loss of forest patches and threshold effects on ecosystem services in southern Madagascar. Ecol Appl 16:440–451
Brazilian Ministry of the Environment – MMA (2017) IOP Publishing PhysicsWeb. http://www.mma.gov.br/biodiversidade/projetos-sobre-a-biodiveridade. Accessed 06 June 2017
Brown KS, Ab’Saber AN (1979) Ice-ages forest refuges and evolution in the Neotropics: correlation of paleoclimatological, geomorphological, and pedological data with modern biological endemism. Paleoclimas 5:1–30
Carnaval AC, Moritz C (2008) Historical climate modelling predicts patterns of current biodiversity in the Brazilian Atlantic forest. J Biogeogr 35:1187–1201. https://doi.org/10.1111/j.1365-2699.2007.01870.x
Carnaval AC, Hickerson MJ, Haddad CFB et al (2009) Stability Predicts Genetic Diversity in the Brazilian Atlantic Forest Hotspot. Science 323:785–789. https://doi.org/10.1126/science.1166955
Carvalho AF, Del Lama MA (2015) Predicting priority areas for conservation from historical climate modelling: stingless bees from Atlantic Forest hotspot as a case study. J Insect Conserv 19:581–587. https://doi.org/10.1007/s10841-015-9780-7
da Rocha-Filho LC, Garofalo CA (2013) Community Ecology of Euglossine Bees in the Coastal Atlantic Forest of São Paulo State, Brazil. J Insect Sci 13:1–19. https://doi.org/10.1673/031.013.2301
da Silva JMC, Tabarelli M (2000) Tree species impoverishment and the future flora of the Atlantic forest of northeast Brazil. Nature 404:72–74. https://doi.org/10.1038/35003563
Darrault RO, Medeiros PCR, Locatelli E, Lopes AV, Machado IC, Schlindwein C (2006) Abelhas Euglossini. In: Pôrto KC, Almeida-Cortez JS, Tabarelli M (eds) Diversidade biológica e conservação da Floresta Atlântica ao norte do Rio São Francisco. Ministério do Meio Ambiente, Brasília, pp 239–253
Dressler RL (1982) Biology of the Orchid Bees (Euglossini). Annu Rev Ecol Syst 13:373–394. https://doi.org/10.1146/annurev.es.13.110182.002105
Dunning JB, Danielson BJ, Pulliam HR (1992) Ecological processes that affect populations in complex landscapes. Oikos 65:169–175
Faria LRR, Melo GAR (2011) A new species of Eufriesea Cockerell (Hymenoptera, Apidae, Euglossina) from northeastern Brazil. Rev Bras Entomol 55:35–39. https://doi.org/10.1590/S0085-56262011000100007
Fischer J, Lindenmayer DB (2002) Small patches can be valuable for biodiversity conservation: two case studies on birds in southeastern Australia. Biol Cons 106:129–136
Fonseca CR, Ganade G, Baldissera R, Becker CG, Boelter CR, Brescovit AD, Campos LM, Fleck T, Fonseca VS, Hartz SM, Joner F, Käffer MI, Leal-Zanchet AM, Marcelli MP, Mesquita AS, Mondin CA, Paz CP, Petry MV, Piovezan FN, Putzke J, Stranz A, Vergara M, Vieira EM (2009) Towards an ecologically sustainable forestry in the Atlantic Forest. Biol Conserv 142:1209–1219
Frankham R, Ballou JD, Briscoe DA (2008) Fundamentos de Genética da Conservação. Sociedade Brasileira de Genética, Ribeirão Preto
Frantine-Silva W, Giangarelli DC, Penha RES, Suzuki KM, Dec E, Gaglianone MC, Alves-dos-Santos I, Sofia SH (2017) Phylogeography and historical demography of the orchid bee Euglossa iopoecila: signs of vicariant events associated to Quaternary climatic changes. Conserv Genet 18:539–552. https://doi.org/10.1007/s10592-016-0905-7
Fundação SOS Mata Atlântica Instituto Nacional de Pesquisas Espaciais (2017) Atlas dos remanescentes florestais da Mata Atlântica período. Instituto Nacional de Pesquisas Espaciais, São Paulo
Galindo-Leal C, Câmara IG (2003) Atlantic Forest hotspot status: an overview. In: Galindo-Leal C, Câmara IG (eds) The Atlantic Forest of South America: biodiversity status, threats, and outlook. Center for Applied Biodiversity Science at Conservation International, Washington
Garraffoni ARS, Moura FR, Lourenço AP (2017) Areas of endemism in the Atlantic Forest: quantitative biogeography insights from orchid bees (Apidae: Euglossini). Apidologie 48:513–522
Giannini TC, Acosta AL, Garófalo CA et al (2012) Pollination services at risk: bee habitats will decrease owing to climate change in Brazil. Ecol Modell 244:127–131. https://doi.org/10.1016/j.ecolmodel.2012.06.035
Giannini TC, Acosta AL, da Silva CI et al (2013) Identifying the areas to preserve passion fruit pollination service in Brazilian Tropical Savannas under climate change. Agric Ecosyst Environ 171:39–46. https://doi.org/10.1016/j.agee.2013.03.003
Goulson D, Nicholls E, Botías C, Rotheray EL (2015) Bee declines driven by combined stress from parasites, pesticides, and lack of flowers. Sci 347:1255957
Haffer J (1969) Speciation in Amazonian Forest Birds. Science 165:131–137. https://doi.org/10.1126/science.165.3889.131
Hammer O, Harper DAT, Ryan PD (2001) PAST: paleontological statistics software package for education and data analysis. Palaeontol Electron. https://doi.org/10.1016/j.bcp.2008.05.025
Holland JM, Smith BM, Storkey J et al (2015) Managing habitats on English farmland for insect pollinator conservation. Biol Conserv 182:215–222. https://doi.org/10.1016/j.biocon.2014.12.009
Hugall A, Moritz C, Moussalli A, Stanisic J (2002) Reconciling paleodistribution models and comparative phylogeography in the Wet Tropics rainforest land snail Gnarosophia bellendenkerensis (Brazier 1875). Proc Natl Acad Sci 99:6112–6117. https://doi.org/10.1073/pnas.092538699
Janzen DH (1971) Euglossine bees as long-distance pollinators of tropical plants. Science 171:203–205
Kevan PG, Viana BF (2003) The global decline of pollination services. Biodiversity 4:3–8. https://doi.org/10.1080/14888386.2003.9712703
Martins FM (2011) Historical biogeography of the Brazilian Atlantic forest and the Carnaval-Moritz model of Pleistocene refugia: what do phylogeographical studies tell us? Biol J Linn Soc 104:499–509. https://doi.org/10.1111/j.1095-8312.2011.01745.x
Minckley RL, Roulston TH (2006) Incidental mutualisms and pollen specialization among bees. In: Waser NM, Ollerton J (eds) Plant-pollinator interactions: from specialization to generalization. The University of Chicago Press, Chicago and London, pp 69–98
Miranda EA, Carvalho AF, Andrade-Silva ACR et al (2015) Natural history and biogeography of Partamona rustica, an endemic bee in dry forests of Brazil. Insect Sociaux 62:255–263
Miranda EA, Batalha-Filho H, Congrains C et al (2016) Phylogeography of Partamona rustica (Hymenoptera, Apidae), an endemic stingless bee from the neotropical dry forest diagonal. PLoS ONE. https://doi.org/10.1371/journal.pone.0164441
Miranda EA, Ferreira KM, Carvalho AT, Martins CF, Fernandes CR, Del Lama MA (2017) Pleistocene climate changes shaped the population structure of Partamona seridoensis (Apidae, Meliponini), an endemic stingless bee from the Neotropical dry forest. PLoS ONE 12(4):e0175725. https://doi.org/10.1371/journal.pone.0175725
Moure JS, Schlindwein C (2002) Uma nova espécie de Euglosssa (Euglossella) Moure do Nordeste do Brasil (Hymenoptera, Apidae). Rev Bras Zool 19:585–588. https://doi.org/10.1590/S0101-81752002000200014
Myers N, Mittermeier RA, Mittermeier CC et al (2000) Biodiversity hotspots for conservation priorities. Nature 403:853–858. https://doi.org/10.1038/35002501
Nemésio A (2009) Orchid bees (Hymenoptera: Apidae) of the Brazilian Atlantic forest. Zootaxa 2041:1–242
Nemésio A, Silveira FA (2006) Edge effects on the orchid-bee fauna (Hymenoptera: Apidae) at a large remnant of Atlantic Rain Forest in southeastern Brazil. Neotrop Entomol 35:313–323. https://doi.org/10.1590/S1519-566X2006000300004
Nemésio A, Silveira FA (2010) Forest Fragments with Larger Core Areas Better Sustain Diverse Orchid Bee Faunas (Hymenoptera: Apidae: Euglossina). Neotrop Entomol 39(4):555–561. https://doi.org/10.1590/S1519-566X2010000400014
Nemésio A, Silva DP, Nabout JC, Varela S (2016) Effects of climate change and habitat loss on a forest-dependent bee species in a tropical fragmented landscape. Insect Conserv Divers. 9:149–160. https://doi.org/10.1111/icad.12154
Oliveira R, Pinto CE, Schlindwein C (2015) Two common species dominate the species-rich Euglossine bee fauna of an Atlantic Rainforest remnant in Pernambuco. Brazil. Braz J Biol. https://doi.org/10.1590/1519-6984.18513
Pemberton RW, Wheeler GS (2006) Orchid bees don’t need orchids: evidence from the naturalization of an orchid bee in Florida. Ecology 87:1995–2001
Phillips SJ, Anderson RP, Schapire RE (2006) Maximum entropy modeling of species geographic distributions. Ecol Modell 190:231–259. https://doi.org/10.1016/j.ecolmodel.2005.03.026
Pijl L, Dodson CH (1966) Orchid Flowers: Their Pollination and Evolution. University of Miami Press, Coral Gables
Pôrto KC, Almeida-Cortez JS, Tabarelli M (2005) Diversidade biológica e conservação da Floresta Atlântica ao norte do Rio São Francisco. Ministério do Meio Ambiente, Brasília
Potts SG, Biesmeijer JC, Kremen C et al (2010) Global pollinator declines: trends, impacts and drivers. Trends Ecol and Evol 25:345–353
QGIS Development Team (2016) QGIS Geographic Information System. Open Source Geospatial Foundation Project. http://qgis.osgeo.org
Ramalho AV, Gaglianone MC, Oliveira ML (2009) Comunidades de abelhas Euglossina (Hymenoptera; Apidae) em fragmentos de Mata Atlântica no Sudeste do Brasil. Rev Bras entomol 53:95–101. https://doi.org/10.1590/S0085-56262009000100022
Ramalho M, Rosa JF, Dantas E Silva M, 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. https://doi.org/10.1007/s13592-012-0189-y
Rebêlo JMM, Silva FS (1999) Distribuição das abelhas Euglossini (Hymenoptera: apidae) no estado do Maranhão, Brasil. An da Soc Entomológica do Bras 28:389–401. https://doi.org/10.1590/S0301-80591999000300003
Ribeiro MC, Metzger JP, Martensen AC et al (2009) The Brazilian Atlantic Forest: how much is left, and how is the remaining forest distributed? Implications for conservation. Biol Conserv 142:1141–1153. https://doi.org/10.1016/j.biocon.2009.02.021
Rocha CFD, Bergalho HG, Alves MAS, Sluys MV (2003) A biodiversidade nos grandes remanescentes florestais do Estado do Rio de Janeiro e nas restingas da Mata Atlântica. RIMA, São Carlos
Rosauer D, Laffan SW, Crisp MD et al (2009) Phylogenetic endemism: a new approach for identifying geographical concentrations of evolutionary history. Mol Ecol 18:4061–4072. https://doi.org/10.1111/j.1365-294X.2009.04311.x
Roubik DW, Hanson PE (2004) Orchid bees from tropical America: Biology and field guide. INBio, Heredia
Silva JMC, Tabarelli M (2001) The future of Atlantic forest in northeastern Brazil. Conserv Biol 15:819–820. https://doi.org/10.1046/j.1523-1739.2001.00014-4.x
Silva CI, Solange CA, Silvia H, Ismar SM (2007) Diversidade de abelhas em Tecoma stans (L.) Kunth (Bignoniaceae): importância na polinização e produção de frutos. Neotrop Entomol 36:331–341
Silva CI, Bordon NG, Rocha Filho LC, Garófalo CA (2012) The importance of plant diversity in maintaining the pollinator bee, Eulaema nigrita (Hymenoptera: Apidae) in sweet passion fruit fields. Rev Biol Trop 60:1553–1565
Silva CI, Marchi P, Aleixo KP, Nunes-Silva B, Freitas BM, Garófalo CA, Imperatriz Fonseca VL, Oliveira PEAM, Alves-dos-Santos I (2014) Manejo dos polinizadores e polinização das flores do maracujazeiro. Instituto de Estudos Avançados da Universidade de São Paulo and Ministério do Meio Ambiente - Brasil. 64 p
Silveira FA, Melo GAR, Almeida EAB (2002) Abelhas brasileiras: sistemática e identificação. Edioria Composição e Arte, Belo Horizonte
Singer R (2001) Flower Morphology and Pollination Mechanism in Three Sympatric Goodyerinae Orchids from Southeastern Brazil. Ann Bot 88:989–997. https://doi.org/10.1006/anbo.2001.1534
Soley-Guardia M, Radosavljevic A, Rivera JL, Anderson RP (2014) The effect of spatially marginal localities in modelling species niches and distributions. J Biogeogr 41:1390–1401. https://doi.org/10.1111/jbi.12297
Solomon SE, Bacci M, Martins J et al (2008) Paleodistributions and comparative molecular phylogeography of leafcutter ants (Atta spp.) provide new insight into the origins of Amazonian diversity. PLoS ONE. https://doi.org/10.1371/journal.pone.0002738
Tscharntke T, Steffan-Dewenter I, Kruess A, Thies C (2002) Contribution of small habitat fragments to conservation of insect communities of grassland-cropland landscapes. Ecol Appl 12:354–363
Vanbergen AJ (2013) Threats to an ecosystem service: pressures on pollinators. Front Ecol Environ 11:251–259
Werneck FP, Costa GC, Colli GR et al (2011) Revisiting the historical distribution of Seasonally Dry Tropical Forests: new insights based on palaeodistribution modelling and palynological evidencegeb. Glob Ecol Biogeogr 20:272–288. https://doi.org/10.1111/j.1466-8238.2010.00596.x
Werneck FP, Nogueira C, Colli GR et al (2012) Climatic stability in the Brazilian Cerrado: implications for biogeographical connections of South American savannas, species richness and conservation in a biodiversity hotspot. J Biogeogr 39:1695–1706. https://doi.org/10.1111/j.1365-2699.2012.02715.x
Willmer PG (2012) Pollinator–plant synchrony tested by climate change. Curr Biol 22:R131–R132
Acknowledgements
We thank to Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq, process 154912/2016-6 and 310178/2015-0) for financial support. We thank to Ariel Fontes and the Msc. Carlos Magno Santos Clemente for technical support.
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Miranda, E.A., Carvalho, A.F., de Jesus Gomes-Miranda, J. et al. Priority areas for conservation of orchid bees (Apidae, Euglossini) in the Atlantic Forest. J Insect Conserv 23, 613–621 (2019). https://doi.org/10.1007/s10841-019-00155-9
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DOI: https://doi.org/10.1007/s10841-019-00155-9