Invasive Africanized honeybees change the structure of native pollination networks in Brazil

Biological Invasions

Volumn 14, Issue 11, 2012, Pages 2369-2378

  de M Santos, Gilberto M ^a   Aguiar, Cândida M L ^a   Genini, Julieta ^b   Martins, Celso F ^c   Zanella, Fernando C V ^d   Mello, Marco A R ^e  

^a DEPARTAMENTO DE CIÊNCIAS BIOLÓGICAS   (Brazil)

^b SÃO PAULO STATE UNIVERSITY UNESP   (Brazil)

^c FEDERAL UNIVERSITY OF PARAÍBA   (Brazil)

^d FEDERAL UNIVERSITY OF CAMPINA GRANDE   (Brazil)

^e UNIVERSITY OF ULM   (Germany)

Author keywords

Apis mellifera; Centrality; Complex networks; Ecosystem services; Modularity; Nestedness; Pollination

Indexed keywords

APICULTURE; BIOLOGICAL INVASION; CAATINGA; HONEYBEE; INVASIVE SPECIES; NESTEDNESS; POLLINATION;

BRAZIL;

APIS MELLIFERA; APIS MELLIFERA SCUTELLATA; APOIDEA;

EID: 84867402537     PISSN: 13873547     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10530-012-0235-8     Document Type: Article

References (47)

1. Aebi A, Neumann P (2011) Endosymbionts and honey bee colony losses? Trends Ecol Evol 26(10): 494. doi: 10. 1016/j. tree. 2011. 06. 008.
2. Aebi A, Vaissière BE, vanEngelsdorp D, Delaplane KS, Roubik DW, Neumann P (2012) Back to the future: Apis versus non-Apis pollination. Trends Ecol Evol 27(3): 142-143. doi: 10. 1016/j. tree. 2011. 11. 017.
3. Aguiar CML (2003) Utilização de recursos florais por abelhas (Hymenoptera, Apoidea) em uma área de caatinga (Itatim, Bahia, Brasil). Rev Bras Zool 20: 457-467.
4. Aguiar CML, Martins CF, Moura ACA (1995) Recursos florais utilizados por abelhas (Hymenoptera, Apoidea) em área de caatinga (São João do Cariri, Paraíba). Revista Nordestina de Biologia 9: 125-131.
5. Aizen MA, Feinsinger P (1994) Habitat fragmentation, native insect pollinators, and feral honey bees in Argentine 'Chaco Serrano'. Ecol Appl 4(2): 378-392. doi: 10. 2307/1941941.
6. Aizen MA, Morales CL, Morales JM (2008) Invasive mutualists erode native pollination webs. PLoS Biol 6(2): e31. doi: 10. 1371/journal. pbio. 0060031.
7. Almeida-Neto M, Guimarães PR, Guimarães PR Jr, Loyola RD, Ulrich W (2008) A consistent metric for nestedness analysis in ecological systems: reconciling concept and measurement. Oikos 117(8): 1227-1239. doi: 10. 1111/j. 2008. 0030-1299. 16644. x.
8. Andrade-Lima D (1981) The Caatinga dominium. Revista Brasileira de Botânica 4: 149-153.
9. Bascompte J, Jordano P (2007) Plant-animal mutualistic networks: the architecture of biodiversity. Annu Rev Ecol Evol Syst 38: 567-593. doi: 10. 1146/annurev. ecolsys. 38. 091206. 095818.
10. Bascompte J, Jordano P, Melian CJ, Olesen JM (2003) The nested assembly of plant-animal mutualistic networks. Proc Nat Acad Sci USA 100(16): 9383-9387. doi: 10. 1073/pnas. 1633576100.
11. Bastolla U, Fortuna MA, Pascual-Garcia A, Ferrera A, Luque B, Bascompte J (2009) The architecture of mutualistic networks minimizes competition and increases biodiversity. Nature 458(7241): U1018-U1091. doi: 10. 1038/nature07950.
12. Bezerra ELS, Machado ICS, Mello MAR (2009) Pollination networks of oil-flowers: a tiny world within the smallest of all worlds. J Anim Ecol 78: 1096-1101. doi: 10. 1111/j. 1365-2656. 2009. 01567. x.
13. Biesmeijer JC, Slaa EJ (2006) The structure of eusocial bee assemblages in Brazil. Apidologie 37(2): 240-258. doi: 10. 1051/apido: 2006014.
14. Biesmeijer JC, Slaa EJ, Castro MS, Viana BF, Kleinert AMP, Imperatriz-Fonseca VL (2005) Connectance of Brazilian social bee: food plant network is influenced by habitat, but not by latitude, altitude or network size. Biota Neotropica 5: online. doi: 10. 1590/S1676-06032005000100010.
15. Blondel J (2003) Guilds or functional groups: does it matter? Oikos 100: 223-231.
16. Brown MJF, Paxton RJ (2009) The conservation of bees: a global perspective. Apidologie 40(3): 410-416. doi: 10. 1051/apido/2009019.
17. Burgos E, Ceva H, Perazzo RPJ, Devoto M, Medan D, Zimmermann M, MarÌa Delbue A (2007) Why nestedness in mutualistic networks? J Theor Biol 249(2): 307-313. doi: 10. 1016/j. jtbi. 2007. 07. 030.
18. Butz-Huryn VN (1997) Ecological impacts of introduced honeybees. Q Rev Biol 72: 275-297.
19. Didham RK, Tylianakis JM, Hutchison MA, Ewers RM, Gemmell NJ (2005) Are invasive species the drivers of ecological change? Trends Ecol Evol 20(9): 470-474. doi: 10. 1016/j. tree. 2005. 07. 006.
20. Dormann CF, Gruber B, Fründ J (2008) Introducing the bipartite package: analyzing ecological networks. R News 8(2): 8-11.
21. Dupont YL, Olesen JM (2009) Ecological modules and roles of species in heathland plant-insect flower visitor networks. J Anim Ecol 78(2): 346-353. doi: 10. 1111/j. 1365-2656. 2008. 01501. x.
22. Dupont YL, Hansen DM, Valido A, Olesen JM (2004) Impact of introduced honey bees on native pollination interactions of the endemic Echium wildpretii (Boraginaceae) on Tenerife, Canary Islands. Biol Conserv 118(3): 301-311. doi: 10. 1016/j. biocon. 2003. 09. 010.
23. Elton C (2001) Animal ecology, reprint edn. The University of Chicago Press, Chicago.
24. Genini J, Morellato LPC, Guimaraes PR, Olesen JM (2010) Cheaters in mutualism networks. Biol Lett. doi: 10. 1098/rsbl. 2009. 1021.
25. Goulson D (2003a) Effects of introduced bees on native ecosystems. Annu Rev Ecol Evol Syst 34(1): 1-26. doi: 10. 1146/annurev. ecolsys. 34. 011802. 132355.
26. Goulson D (2003b) Effects of introduced bees on native ecosystems. Annu Rev Ecol Evol Syst 34(1): 1-26.
27. Guimarães PR, Guimarães P (2006) Improving the analyses of nestedness for large sets of matrices. Environ Model Softw 21: 1512-1513.
28. Guimerà R, Amaral LAN (2005) Functional cartography of complex metabolic networks. Nature 433: 895-900.
29. Jordano P (1987) Patterns of mutualistic interactions in pollination and seed dispersal-connectance, dependence asymmetries, and coevolution. Am Nat 129(5): 657-677.
30. Jordano P, Bascompte J, Olesen JM (2003) Invariant properties in coevolutionary networks of plant-animal interactions. Ecol Lett 6(1): 69-81.
31. Lopezaraiza-Mikel ME, Hayes RB, Whalley MR, Memmott J (2007) The impact of an alien plant on a native plant-pollinator network: an experimental approach. Ecol Lett 10(7): 539-550. doi: 10. 1111/j. 1461-0248. 2007. 01055. x.
32. Mello MAR, Marquitti FMD, Guimarães PR Jr, Kalko EKV, Jordano P, Aguiar MAM (2011a) The missing part of seed dispersal networks: structure and robustness of bat-fruit interactions. PLoS One Accepted with revision.
33. Mello MAR, Marquitti FMD, Guimarães PR Jr, Kalko EKV, Jordano P, Aguiar MAM (2011b) The modularity of seed dispersal: differences in structure and robustness between bat- and bird-fruit networks. Oecologia Accepted with revision.
34. Mello MAR, Marquitti FMD, Guimarães PR Jr, Kalko EKV, Jordano P, de Aguiar MAM (2011c) The missing part of seed dispersal networks: structure and robustness of bat-fruit interactions. PLoS ONE 6(2): e17395. doi: 10. 1371/journal. pone. 0017395.
35. Michener CD (1975) The Brazilian bee problem. Annu Rev Entomol 20: 399-416.
36. Myers N, Mittermeier RA, Mittermeier CG, Fonseca GAB, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 403: 853-858.
37. Nooy W, Mrvar A, Batagelj V (2005) Exploratory social network analysis with Pajek. Cambridge University Press, New York.
38. Olesen JM, Bascompte J, Dupont YL, Jordano P (2007) The modularity of pollination networks. Proc Nat Acad Sci USA 104(50): 19891-19896. doi: 10. 1073/pnas. 0706375104.
39. Ollerton J, Price V, Armbruster WS, Memmott J, Watts S, Waser NM, Totland Ø, Goulson D, Alarcón R, Stout JC, Tarrant S (2012) Overplaying the role of honey bees as pollinators: a comment on Aebi and Neumann (2011). Trends Ecol Evol 27(3): 141-142. doi: 10. 1016/j. tree. 2011. 12. 001.
40. Padron B, Traveset A, Biedenweg T, Diaz D, Nogales M, Olesen JM (2009) Impact of alien plant invaders on pollination networks in two archipelagos. PLoS ONE 4(7): e6275. doi: 10. 1371/journal. pone. 0006275.
41. Prado DE (2000) Seasonally dry forests of tropical South America: from forgotten ecosystems to a new phytogeographic unit. Edinb J Bot 57: 437-461.
42. Prado DE, Gibbs PE (1993) Patterns of species distributions in the dry seasonal forest of South America. Ann Mo Bot Gard 80: 902-927.
43. Romanuk TN, Zhou Y, Brose U, Berlow EL, Williams RJ, Martinez ND (2009) Predicting invasion success in complex ecological networks. Philos Trans R Soc B Biol Sci 364: 1743-1754. doi: 10. 1098/rstb. 2008. 0286.
44. Takhtajan A (1986) Floristic regions of the world. University of California Press, Berkeley.
45. Walker BH (1992) Biodiversity and ecological redundancy. Conserv Biol 6(1): 18-23. doi: 10. 1046/j. 1523-1739. 1992. 610018. x.
46. Zanella FCV, Martins CF (2003) Abelhas da caatinga: biogeografia, ecologia e conservação. In: Leal IR, Tabarelli M, Silva JMC (eds) Ecologia e conservação da caatinga. Editora Universitária da UFPE, Recife, p 804.
47. Zar JH (1996) Biostatistical analysis. Prentice-Hall, New Jersey.