Responses of bees to habitat loss in fragmented landscapes of Brazilian Atlantic Rainforest
- 936 Downloads
Loss of natural habitat can isolate pollinator populations and negatively affect sexual reproduction of animal-pollinated plants.
We evaluated how the loss of natural forest affects pollinator diversity in the understory of the Atlantic Rainforest in Northeastern Brazil.
We focused on bees, the main group of pollinators for angiosperms. We assessed how changes in forest cover at regional (36 km2) and local (0.36 km2) scales affect bee richness and abundance.
We sampled 492 bees from 59 species, of which 58 % were above ground nesting species and 73 % exhibited some level of sociality. Our results show that the loss of forest had negative effects on understory bee abundance, which was particularly accentuated for species that nest above ground. However, for social bees the effect of changes in forest cover at a local scale depended on regional forest cover, negative effects being only detected when landscapes had at least 35 % of forest. For bee richness, the null model was among the best models bringing considerable uncertainty about landscape effects on bee richness.
These findings suggest that management strategies and conservation practices must integrate proper actions that consider both local and regional scales. For existing fragmented landscapes, it is important to increase forest availability at the regional scale, while also maintaining high environmental heterogeneity at the local scale. We believe that with proper landscape planning this multiscalar approach can be not only more effective, but also easier to implement.
KeywordsPollinators Forest understory Tropical Landscape changes Multiscalar approach Bahia Brazil
We want to thank the financial research support by INOMEP-PRONEX-CNPQ, and essential financial support by FAPESB, CNPQ and CAPES. Jesus Aguirre-Gutierrez helped with forest cover calculations. Dra. Favízia F. Oliveira and MSc. Thiago Mahlmann aided in bee identification and information about bee nests and sociability. Dr. Luciano E. Lopes, Dr. Jean Paul Metzger, Dra. Astrid M. P. Kleinert, Dra. Camila Magalhães Pigozzo and Dr. Eduardo Mariano Neto add helpful and valuable comments in previous versions of this manuscript. Dr. Cory S. Sheffield add helpful comments and did the English revision. We also thank the Landscape Ecology Editor and the two anonymous reviewers for their excellent contributions to the manuscript.
- Billeter R, Liira J, Bailey D, Bugter R, Arens P, Augenstein I, Aviron S, Baudry J, Bukacek R, Burel F, Cerny M, De Blust G, De Cock R, Diekötter T, Dietz H, Dirksen J, Dormann C, Durka W, Frenzel M, Hamersky R, Hendrickx F, Herzog F, Klotz S, Koolstra B, Lausch A, Le Coeur D, Maelfait JP, Opdam P, Roubalova M, Schermann A, Schermann N, Schmidt T, Schweiger O, Smulders MJM, Speelmans M, Simova P, Verboom J, van Wingerden W, Zobel M, Edwards PJ (2008) Indicators for biodiversity in agricultural landscapes: a pan-European study. J Appl Ecol 45:141–150CrossRefGoogle Scholar
- Burnham KP, Anderson DR (2002) Model selection and multi-model inference: a practical information-theoretic approach, 2nd edn. Springer, NewYorkGoogle Scholar
- Dormann CF, Schweiger O, Augenstein I, Bailey D, Billeter R, Blust G, DeFilippi R, Frenzel M, Hendrickx F, Herzog F, Klotz S, Liira J, Maelfait JP, Schmidt T, Speelmans M, van Wingerden W, Zobel M (2007) Effects of landscape structure and land-use intensity on similarity of plant and animal communities. Global Ecol Biogeogr 16:774–787CrossRefGoogle Scholar
- Garibaldi LA, Steffan-Dewenter I, Kremen C, Morales JM, Bommarco R, Cunningham SA, Carvalheiro LG, Chacoff NP, Dudenhöffer JH, Greenleaf SS, Holzschuh A, Isaacs R, Krewenka K, Mandelik Y, Mayfield MM, Morandin LA, Potts SG, Ricketts TH, Szentgyörgyi H, Viana BF, Westphal C, Winfree R, Klein AM (2011) Stability of pollination services decreases with isolation from natural areas despite honey bee visits. Ecol Lett 14:1062–1072CrossRefPubMedGoogle Scholar
- Garibaldi LA, Steffan-Dewenter I, Winfree R, Aizen MA, Bommarco R, Cunningham SA, Kremen C, Carvalheiro LG, Harder LD, Afik O, Bartomeus I, Benjamin F, Boreux V, Cariveau D, Chacoff NP, Dudenhöffer JH, Freitas BM, Ghazoul J, Greenleaf S, Hipólito J, Holzschuh A, Howlett B, Isaacs R, Javorek SK, Kennedy CM, Krewenka KM, Krishnan S, Mandelik Y, Mayfield MM, Motzke I, Munyuli T, Nault BA, Otieno M, Petersen J, Pisanty G, Potts SG, Rader R, Ricketts TH, Rundlöf M, Seymour CL, Schüepp C, Szentgyörgyi H, Taki H, Tscharntke T, Vergara CH, Viana BF, Wanger TC, Westphal C, Williams N, Klein AM (2013) Wild pollinators enhance fruit set of crops regardless of honey-bee abundance. Science 339:1608–1611CrossRefPubMedGoogle Scholar
- Hendrickx F, Maelfait JP, van Wingerden W, Schweiger O, Speelmans M, Aviron S, Augenstein I, Billeter R, Bailey D, Bukacek R, Burel F, Diekötter T, Dirksen J, Herzog F, Liira J, Roubalova M, Vandomme V, Bugter R (2007) How landscape structure, land-use intensity and habitat diversity affect components of total arthropod diversity in agricultural landscapes. J Appl Ecol 44:340–351CrossRefGoogle Scholar
- Kennedy CM, Lonsdorf E, Neel MC, Williams NM, Ricketts TH, Winfree R, Bommarco R, Brittain C, Burley AL, Cariveau D, Carvalheiro LG, Chacoff NP, Cunningham SA, Danforth BN, Dudenhöffer J, Elle E, Gaines HR, Garibaldi LA, Gratton C, Holzschuh A, Isaacs R, Javorek SK, Jha S, Klein AM, Krewenka K, Mandelik Y, Mayfield MM, Morandin L, Neame LA, Otieno M, Park M, Potts SG, Rundlöf M, Saez A, Steffan-Dewenter I, Taki H, Viana BF, Westphal C, Wilson JK, Greenleaf SS, Kremen C (2013) A global quantitative synthesis of local and landscape effects on wild bee pollinators in agroecosystems. Ecol Lett 16:584–599CrossRefPubMedGoogle Scholar
- Kremen C, Williams NM, Aizen MA, Gemmill-Herren B, LeBuhn G, Minckley R, Packer L, Potts SG, Roulston T, Steffan-Dewenter I, Vazquez D, Winfree R, Adams L, Crone EE, Greenleaf SS, Keitt TH, Klein A, Regetz J, Ricketts T (2007) Pollination and other ecosystem services produced by mobile organisms: a conceptual framework for the effects of land use change. Ecol Lett 10:299–314CrossRefPubMedGoogle Scholar
- McGarigal K, Marks BJ (1995) Fragstats: spatial pattern analysis program for quantifying landscape structure. USDA Forest Service General Technical Report PNW-GTR-351, CornvallisGoogle Scholar
- Michener CD (2007) The bees of the world, 2nd edn. Johns Hopkins University Press, BaltimoreGoogle Scholar
- Moure JS, Urban D, Melo GAR (2012) Catalogue of bees (Hymenoptera, Apoidea) in the neotropical region—online version. Available at http://www.moure.cria.org.br/catalogue
- R Development Core Team (2009) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
- Ramalho M (2004) Stingless bees and mass flowering trees in the canopy of Atlantic Forest: a tight relationship. Act Bot Bras 18(1):37–47Google Scholar
- Ricketts TH, Regetz J, Steffan-Dewenter I, Cunningham SA, Kremen C, Bogdanski A, Gemmill-Herren B, Greenleaf SS, Klein AM, Mayfield MM, Morandin LA, Ochieng A, Viana BF (2008) Landscape effects on crop pollination services: are there general patterns? Ecol Lett 11(5):499–515CrossRefPubMedGoogle Scholar
- Roubik DW (1995) Pollination of cultivated plants in the tropics. food and agricultural organization of the United Nations. Agricultural Bulletin No. 118, RomeGoogle Scholar
- Schueepp C, Herzog F, Entling MH (2014) Disentangling multiple drivers of pollination in a landscape-scale experiment. Proc R Soc B 281:1–8Google Scholar
- Schweiger O, Maelfait JP, van Wingerden W, Hendrickx F, Billeter R, Speelmans M, Augenstein I, Aukema B, Aviron S, Bailey D, Bukacek R, Burel F, Diekötter T, Dirksen J, Frenzel M, Herzog F, Liira J, Roubalova M, Bugter R (2005) Quantifying the impact of environmental factors on arthropod communities in agricultural landscapes across organizational levels and spatial scales. J Appl Ecol 42:1129–1139CrossRefGoogle Scholar
- 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 12:354–363Google Scholar
- Veloso HP, Filho ALRR, Lima JCA (1991) Classificação da vegetação brasileira, adaptada a um sistema universal. Fundação Instituto Brasileiro de Geografia e Estatística – IBGE (Classification of Brazilian vegetation adapted to a universal system. Brazilian Institute of Geography and Statistics - IBGE). Rio de JaneiroGoogle Scholar
- Viana BF, Boscolo D, Neto EM, Lopes LE, Lopes AV, Ferreira PA, Pigozzo CM, Primo LM (2012) How well do we understand landscape effects on pollinators and pollination services? J Pollinat Ecol 7(5):31–41Google Scholar