Advertisement

Landscape Ecology

, Volume 30, Issue 10, pp 2067–2078 | Cite as

Responses of bees to habitat loss in fragmented landscapes of Brazilian Atlantic Rainforest

  • Patrícia A. Ferreira
  • Danilo Boscolo
  • Luísa G. Carvalheiro
  • Jacobus C. Biesmeijer
  • Pedro L. B. Rocha
  • Blandina F. Viana
Research Article

Abstract

Context

Loss of natural habitat can isolate pollinator populations and negatively affect sexual reproduction of animal-pollinated plants.

Objective

We evaluated how the loss of natural forest affects pollinator diversity in the understory of the Atlantic Rainforest in Northeastern Brazil.

Methods

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.

Results

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.

Conclusions

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.

Keywords

Pollinators Forest understory Tropical Landscape changes Multiscalar approach Bahia Brazil 

Notes

Acknowledgments

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.

Supplementary material

10980_2015_231_MOESM1_ESM.doc (143 kb)
Supplementary material 1 (DOC 143 kb)

References

  1. Andrén H (1994) Effects of habitat fragmentation on birds and mammals in landscapes with different proportions of suitable habitat: a review. Oikos 71:355–366CrossRefGoogle Scholar
  2. Bawa KS (1990) Plant-pollinator interactions in tropical rain forests. Ann Rev Ecol Syst 21:399–422CrossRefGoogle Scholar
  3. 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
  4. Boscolo D, Metzger JP (2011) Isolation determines patterns of species presence in highly fragmented landscapes. Ecography 34:1018–1029CrossRefGoogle Scholar
  5. Brosi BJ, Daily GC, Ehrlich PR (2007) Bee community shifts with landscape context in a tropical countryside. Ecol Appl 17(2):418–430CrossRefPubMedGoogle Scholar
  6. Brosi BJ, Daily GC, Shih TM, Oviedo F, Durán G (2008) The effects of forest fragmentation on bee communities in tropical countryside. J Appl Ecol 45(3):773–783CrossRefGoogle Scholar
  7. Burnham KP, Anderson DR (2002) Model selection and multi-model inference: a practical information-theoretic approach, 2nd edn. Springer, NewYorkGoogle Scholar
  8. Cane JH, Minckley RL, Kervin LJ, Roulston TH, Williams NM (2006) Complex responses within a desert bee guild (Hymenoptera: apiformes) to urban habitat fragmentation. Ecol Appl 16(2):632–644CrossRefPubMedGoogle Scholar
  9. Crawley MJ (2007) The R book. Wiley, Chichester, p 952CrossRefGoogle Scholar
  10. 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
  11. Ebeling A, Klein AM, Schumacher J, Weisser WW, Tscharntke T (2008) How does plant richness affect pollinator richness and temporal stability of flower visits? Oikos 117(12):1808–1815CrossRefGoogle Scholar
  12. Ferreira PA, Boscolo D, Viana BF (2013) What do we know about the effects of landscape changes on plant–pollinator interaction networks? Ecol Indic 31:35–40CrossRefGoogle Scholar
  13. Fontaine C, Dajoz I, Meriguet J, Loreau M (2006) Functional diversity of plant–pollinator interaction webs enhances the persistence of plant communities. PLoS Biol 4:129–135CrossRefGoogle Scholar
  14. 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
  15. 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
  16. Garibaldi LA, Carvalheiro LG, Leonhardt SD, Ma Aizen, Blaauw BR, Isaacs R, Kuhlmann M, Kleijn D, Klein AM, Kremen C, Morandin L, Scheper J, Winfree R (2014) From research to action: practices to enhance crop yield through wild pollinators. Front Ecol Environ 12:439–447CrossRefGoogle Scholar
  17. Gathmann A, Tscharntke T (2002) Foraging ranges of solitary bees. J Anim Ecol 71(5):757–764CrossRefGoogle Scholar
  18. Ghazoul J, McLeish M (2001) Reproductive ecology of tropical forest trees in logged and fragmented habitats in Thailand and Costa Rica. Plant Ecol 153(1–2):335–345CrossRefGoogle Scholar
  19. Grundel R, Jean R, Frohnapple K, Glowacki G, Scott P, Pavlovic N (2010) Floral and nesting resources, habitat structure, and fire influence bee distribution across an open-forest gradient. Ecol Appl 20(6):1678–1692CrossRefPubMedGoogle Scholar
  20. 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
  21. Hoehn P, Tscharntke T, Tylianakis JM, Steffan-Dewenter I (2008) Functional group diversity of bee pollinators increases crop yield. Proc R Soc London B 275(1648):2283–2291CrossRefGoogle Scholar
  22. Hudewenz A, Klein AM (2013) Competition between honey bees and wild bees and the role of nesting resources in a nature reserve. J Insect Conserv 17:1275–1283CrossRefGoogle Scholar
  23. Jackson HB, Fahrig L (2012) What size is a biologically relevant landscape? Landscape Ecol 27:929–941CrossRefGoogle Scholar
  24. 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
  25. Klein AM, Vaissière BE, Cane JH, Steffan-Dewenter I, Cunningham SA, Kremen C, Tscharntke T (2007) Importance of pollinators in changing landscapes for world crops. Proc R Soc London B 274(1608):303–313CrossRefGoogle Scholar
  26. 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
  27. Lander TA, Boshier DH, Harris SA (2010) Fragmented but not isolated: contribution of single trees, small patches and long-distance pollen flow to genetic connectivity for Gomortega keule, an endangered Chilean tree. Biol Conserv 143(11):2583–2590CrossRefGoogle Scholar
  28. Lopes LE, Buzato S (2007) Variation in pollinator assemblages in a fragmented landscape and its effects on reproductive stages of a self-incompatible treelet, Psychotria suterella (Rubiaceae). Oecologia 154:305–314CrossRefPubMedGoogle Scholar
  29. 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
  30. McIntyre NE, Wiens JA (1999) How does habitat patch size affect animal movement? An experiment with darkling beetles. Ecology 80(7):2261–2270CrossRefGoogle Scholar
  31. Michener CD (2007) The bees of the world, 2nd edn. Johns Hopkins University Press, BaltimoreGoogle Scholar
  32. Moreira EF, Boscolo D, Viana BF (2015) Spatial heterogeneity regulates plant-pollinator networks across multiple landscape scales. PLoS ONE 10(4):e0123628PubMedCentralCrossRefPubMedGoogle Scholar
  33. Morreale SJ, Sullivan KL (2010) Community-level enhancements of biodiversity and ecosystem services. Front Earth Sci China 4(1):14–21CrossRefGoogle Scholar
  34. 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
  35. Murray TE, Fitzpatrick U, Byrne A, Fealy R, Brown MJF, Paxton RJ (2012) Local-scale factors structure wild bee communities in protected areas. J Appl Ecol 49:998–1008CrossRefGoogle Scholar
  36. Nazareno AG, Carvalho D (2009) What the reasons for no inbreeding and high genetic diversity of the neotropical fig tree Ficus arpazusa? Conserv Genet 10:1789–1793CrossRefGoogle Scholar
  37. Ollerton J, Winfree R, Tarrant S (2011) How many flowering plants are pollinated by animals? Oikos 120:321–326CrossRefGoogle Scholar
  38. Olschewski R, Klein AM, Tscharntke T (2010) Economic trade-offs between carbon sequestration, timber production, and crop pollination in tropical forested landscapes. Ecol Complex 7(3):314–319CrossRefGoogle Scholar
  39. Osborne JL, Clark SJ, Morris RJ, Williams IH, Riley JR, Smith AD, Reynolds DR, Edwards AS (1999) A landscape-scale study of bumble bee foraging range and constancy, using harmonic radar. J Appl Ecol 36:519–533CrossRefGoogle Scholar
  40. Pardini R, Bueno AA, Gardner TA, Prado PI, Metzger JP (2010) Beyond the fragmentation threshold hypothesis: regime shifts in biodiversity across fragmented landscapes. PLoS ONE 5(10):e13666PubMedCentralCrossRefPubMedGoogle Scholar
  41. Peel MC, Finlayson BL, Mcmahon TA (2007) Updated world map of the Köppen–Geiger climate classification. Hydrol Earth Syst Sci 11:1633–1644CrossRefGoogle Scholar
  42. Potts SG, Petanidou T, Roberts S, O’Toole C, Hulbert A, Willmer P (2006) Plant–pollinator biodiversity and pollination services in a complex Mediterranean landscape. Biol Cons 29:519–529CrossRefGoogle Scholar
  43. Potts SG, Biesmeijer JC, Kremen C, Neumann P, Schweiger O, Kunin WE (2010) Global pollinator declines: trends, impacts and drivers. Trend Ecol Evol 25:345–353CrossRefGoogle Scholar
  44. R Development Core Team (2009) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  45. 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
  46. 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(6):1141–1153CrossRefGoogle Scholar
  47. Ricketts TH (2004) Tropical forest fragments enhance pollinator activity in nearby coffee crops. Conserv Biol 18(5):1262–1271CrossRefGoogle Scholar
  48. 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
  49. Roubik DW (1995) Pollination of cultivated plants in the tropics. food and agricultural organization of the United Nations. Agricultural Bulletin No. 118, RomeGoogle Scholar
  50. 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
  51. 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
  52. Schweiger O, Musche M, Bailey D, Billeter R, Diekötter T, Hendrickx F, Herzog F, Liira J, Maelfait JP, Speelmans M, Dziock F (2007) Functional richness of local hoverfly communities (Diptera, Syrphidae) in response to land use across temperate Europe. Oikos 116:461–472CrossRefGoogle Scholar
  53. Sheffield CS, Kevan PG, Westby SM, Smith RF (2008) Diversity of cavity-nesting bees (Hymenoptera: Apoidea) within apple orchards and wild habitats in the Annapolis Valley, Nova Scotia, Canada. Can Entomol 140:235–249CrossRefGoogle Scholar
  54. Steffan-Dewenter I, Munzenberg U, Burger C, Thies C, Tscharntk T (2002) Scale-dependent effects of landscape context on three pollinator guilds. Ecology 83(5):1421–1432CrossRefGoogle Scholar
  55. Suni SS, Brosi BJ (2012) Population genetics of orchid bees in a fragmented tropical landscape. Conserv Genet 13:323–332CrossRefGoogle Scholar
  56. Tabarelli M, Lopes AV, Peres CA (2008) Edge-effects drive tropical forest fragments towards an early-successional system. Biotropica 40(6):657–661CrossRefGoogle Scholar
  57. Taki H, Kevan PG (2007) Does habitat loss affect the communities of plants and insects equally in plant—pollinator interactions? Preliminary findings. Biodivers Conserv 16(11):3147–3161CrossRefGoogle Scholar
  58. Tscharntke T, Brandl R (2004) Plant-insect interactions in fragmented landscapes. Annu Rev Entmol 49:405–430CrossRefGoogle Scholar
  59. 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
  60. 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
  61. 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
  62. Williams NM, Crone EE, Roulston TH, Minckley RL, Packer L, Potts SG (2010) Ecological and life-history traits predict bee species responses to environmental disturbances. Biol Conserv 143(10):2280–2291CrossRefGoogle Scholar
  63. Winfree R, Griswold T, Kremen C (2007) Effect of human disturbance on bee communities in a forested ecosystem. Conserv Biol 21(1):213–223CrossRefPubMedGoogle Scholar
  64. Winfree R, Aguilar R, Vazquez DP, Lebuhn G, Aizen M (2009) A meta-analysis of bees’ responses to anthropogenic disturbance. Ecology 90(8):2068–2076CrossRefPubMedGoogle Scholar
  65. Winfree R, Bartomeus I, Cariveau DP (2011) Native pollinators in anthropogenic habitats. Annu Rev Ecol Evol Syst 42:1–22CrossRefGoogle Scholar
  66. Zurbuchen A, Landert L, Klaiber J, Müller A, Hein S, Dorn S (2010) Maximum foraging ranges in solitary bees: only few individuals have the capability to cover long foraging distances. Biol Conserv 143(3):669–676CrossRefGoogle Scholar
  67. Zuur A, Ieno EN, Walker N, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. Springer, New YorkCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2015

Authors and Affiliations

  • Patrícia A. Ferreira
    • 1
  • Danilo Boscolo
    • 1
  • Luísa G. Carvalheiro
    • 2
    • 3
    • 4
  • Jacobus C. Biesmeijer
    • 3
    • 5
  • Pedro L. B. Rocha
    • 6
  • Blandina F. Viana
    • 6
  1. 1.Biology Department, Faculty of Philosophy, Sciences and LettersUniversity of São PauloRibeirão PretoBrazil
  2. 2.School of BiologyUniversity of LeedsLeedsUK
  3. 3.Naturalis Biodiversity CenterLeiden UniversityLeidenThe Netherlands
  4. 4.Departament of EcologyUniversity of BrasíliaBrasíliaBrazil
  5. 5.Institute for Biodiversity and Ecosystem DynamicsUniversity of AmsterdamAmsterdamThe Netherlands
  6. 6.Biology InstituteFederal University of BahiaSalvadorBrazil

Personalised recommendations