Invasive Africanized honeybees change the structure of native pollination networks in Brazil
Tóm tắt
The Africanized honeybee Apis mellifera (AHB) is an invasive species spread over all Brazilian biomes, which has negative impacts on native bee populations, but whose impacts on native plants are still controversial. In order to understand how its impacts extend to the pollination service at the community level, we studied the AHB and its interactions in a multi-species context using network theory. We analyzed six pollination networks from the Brazilian Caatinga, a xeric biome where beekeeping is increasing very quickly. The AHB occupied a central position in all networks, as it was responsible for a large share of the interactions observed (14 ± 7 %) and bound together different modules. By simulating the removal of the AHB from each network, we observed no effects on connectance, but a strong decrease in nestedness (−23 ± 19 %) and an increase in modularity (8 ± 5 %). The robustness of networks to cumulative random extinctions was on average not affected. In summary, our evidence points out that the AHB induces significant changes in the structure of native pollination networks, mainly by making them more cohesive and monopolizing many interactions. Although the AHB did not affect network robustness, its net impact on the pollination service may be negative, because this invasive species is very generalistic and may not be an efficient pollinator for some native plants.
Tài liệu tham khảo
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
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
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
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
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
Aizen MA, Morales CL, Morales JM (2008) Invasive mutualists erode native pollination webs. PLoS Biol 6(2):e31. doi:10.1371/journal.pbio.0060031
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
Andrade-Lima D (1981) The Caatinga dominium. Revista Brasileira de Botânica 4:149–153
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
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
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
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
Biesmeijer JC, Slaa EJ (2006) The structure of eusocial bee assemblages in Brazil. Apidologie 37(2):240–258. doi:10.1051/apido:2006014
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
Blondel J (2003) Guilds or functional groups: does it matter? Oikos 100:223–231
Brown MJF, Paxton RJ (2009) The conservation of bees: a global perspective. Apidologie 40(3):410–416. doi:10.1051/apido/2009019
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
Butz-Huryn VN (1997) Ecological impacts of introduced honeybees. Q Rev Biol 72:275–297
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
Dormann CF, Gruber B, Fründ J (2008) Introducing the bipartite package: analyzing ecological networks. R News 8(2):8–11
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
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
Elton C (2001) Animal ecology, reprint edn. The University of Chicago Press, Chicago
Genini J, Morellato LPC, Guimaraes PR, Olesen JM (2010) Cheaters in mutualism networks. Biol Lett. doi:10.1098/rsbl.2009.1021
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
Goulson D (2003b) Effects of introduced bees on native ecosystems. Annu Rev Ecol Evol Syst 34(1):1–26
Guimarães PR, Guimarães P (2006) Improving the analyses of nestedness for large sets of matrices. Environ Model Softw 21:1512–1513
Guimerà R, Amaral LAN (2005) Functional cartography of complex metabolic networks. Nature 433:895–900
Jordano P (1987) Patterns of mutualistic interactions in pollination and seed dispersal—connectance, dependence asymmetries, and coevolution. Am Nat 129(5):657–677
Jordano P, Bascompte J, Olesen JM (2003) Invariant properties in coevolutionary networks of plant-animal interactions. Ecol Lett 6(1):69–81
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
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
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
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
Michener CD (1975) The Brazilian bee problem. Annu Rev Entomol 20:399–416
Myers N, Mittermeier RA, Mittermeier CG, Fonseca GAB, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 403:853–858
Nooy W, Mrvar A, Batagelj V (2005) Exploratory social network analysis with Pajek. Cambridge University Press, New York
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
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
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
Prado DE (2000) Seasonally dry forests of tropical South America: from forgotten ecosystems to a new phytogeographic unit. Edinb J Bot 57:437–461
Prado DE, Gibbs PE (1993) Patterns of species distributions in the dry seasonal forest of South America. Ann Mo Bot Gard 80:902–927
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
Takhtajan A (1986) Floristic regions of the world. University of California Press, Berkeley
Walker BH (1992) Biodiversity and ecological redundancy. Conserv Biol 6(1):18–23. doi:10.1046/j.1523-1739.1992.610018.x
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
Zar JH (1996) Biostatistical analysis. Prentice-Hall, New Jersey