Abstract
Seed dispersal plays a central role in plant ecology. Among animals, birds are particularly important seed dispersers, often incorporating exotic plants into their diets and facilitating their integration in the communities. Network theory offers a highly informative framework to study the structural and functional attributes of complex interactions networks. We used information from bird fecal samples to build a quantitative seed dispersal network for the last fragment of native laurel forest in the island of São Miguel—Azores with three specific objectives: (1) to assess the integration of exotic seeds into seed dispersal; (2) to evaluate the impact of exotic plants in network structure; (3) to test the potential of an exotic species to reduce the seed dispersal of a co-occurring native, via competition for seed dispersers. The seed dispersal network was based on the analysis of 1,121 droppings and described 74 unique interactions between 41 plant species and 7 bird species. Exotic seeds deeply infiltrated into the seed dispersal network forming the majority (59 %) of seeds in the droppings and including those of three globally invasive plants. Overall, birds depended equally on native and exotic fruits despite the lower abundance of the latter in the study area. In an experiment, birds did not show a preference for fruits of the exotic Leycesteria formosa over the native Vaccinium cylindraceum consuming them equally. However, the presence of the exotic plant negatively affected the number of native seeds dispersed, by diverting some of the consumers of the native fruits. Taken altogether the results reveal an alarming invasion level of seed dispersal systems in one of the last remnant native forests of the Azores.
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References
Aslan CE, Rejmánek M (2010) Avian use of introduced plants: ornithologist records illuminate interspecific associations and research needs. Ecol Appl 20(4):1005–1020. doi:10.1890/08-2128.1
Bartuszevige AM, Gorchov DL (2006) Avian seed dispersal of an invasive shrub. Biol Invasions 8(5):1013–1022. doi:10.1007/s10530-005-3634-2
Bascompte J, Jordano P, Olesen J (2006) Asymmetric coevolutionary networks facilitate biodiversity maintenance. Science 312:431–433. doi:10.1126/science.1123412
Berlow EL (1999) Strong effects of weak interactions in ecological communities. Nature 398(6725):330–334
Bersier LF, Banasek-Richter C, Cattin MF (2002) Quantitative descriptors of food-web matrices. Ecology 83(9):2394–2407. doi:10.2307/3071801
Blendinger PG, Villegas M (2011) Crop size is more important than neighborhood fruit availability for fruit removal of Eugenia uniflora (Myrtaceae) by bird seed dispersers. Plant Ecol 212(5):889–899. doi:10.1007/s11258-010-9873-z
Buckley YM, Anderson S, Catterall CP, Corlett RT, Engel T, Gosper CR, Nathan R, Richardson DM, Setter M, Spiegel O, Vivian-Smith G, Voigt FA, Weir JES, Westcott DA (2006) Management of plant invasions mediated by frugivore interactions. J Appl Ecol 43(5):848–857. doi:10.1111/j.1365-2664.2006.01210.x
Calviño-Cancela M (2011) Simplifying methods to assess site suitability for plant recruitment. Plant Ecol 212(8):1375–1383. doi:10.1007/s11258-011-9913-3
Carlo TA (2005) Interspecific neighbors change seed dispersal pattern of an avian-dispersed plant. Ecology 86(9):2440–2449. doi:10.1890/04-1479
Carvalheiro LG, Barbosa ERM, Memmott J (2008) Pollinator networks, alien species and the conservation of rare plants: Trinia glauca as a case study. J Appl Ecol 45(5):1419–1427. doi:10.1111/j.1365-2664.2008.01518.x
Ceia R, Heleno R, Ramos J (2009) Summer abundance and ecological distribution of passerines in native and exotic forests in São Miguel, Azores. Ardeola 56(1):25–39
Ceia RS, Sampaio HL, Parejo SH, Heleno RH, Arosa ML, Ramos JA, Hilton GM (2011) Throwing the baby out with the bathwater: does laurel forest restoration remove a critical winter food supply for the critically endangered Azores bullfinch? Biol Invasions 13:93–104. doi:10.1007/s10530-010-9792-x
Chittka L, Schurkens S (2001) Successful invasion of a floral market—an exotic Asian plant has moved in on Europe’s river-banks by bribing pollinators. Nature 411(6838):653. doi:10.1038/35079676
Cordeiro NJ, Patrick DAG, Munisi B, Gupta V (2004) Role of dispersal in the invasion of an exotic tree in an East African submontane forest. J Trop Ecol 20:449–457. doi:10.1017/s026646740400152x
Côrtes MC, Cazetta E, Staggemeier VG, Galetti M (2009) Linking frugivore activity to early recruitment of a bird dispersed tree, Eugenia umbelliflora (Myrtaceae) in the Atlantic rainforest. Austral Ecol 34(3):249–258. doi:10.1111/j.1442-9993.2009.01926.x
Dias E, Elias R, Melo C, Mendes C (2007) Biologia e ecologia das florestas das Ilhas—Açores. In: Silva JS (ed) Açores e Madeira: a floresta das Ilhas, vol 6. Publico, Fundação Luso-Americana, Lisbon, pp 51–80
Dormann C, Gruber B, Frund J (2008) Introducing the bipartite package: analysing ecological networks. R News 8(2):8–11
Dormann CF, Fründ J, Blüthgen N, Gruber B (2009) Indices, graphs and null models: analyzing bipartite ecological networks. Open J Ecol 2:7–24
Duffy JE, Carinale BJ, France KE, McIntyre PB, Thébault E, Loreau M (2007) The functional role of biodiversity in ecosystems: incorporating trophic complexity. Ecol Lett 10(6):522–538. doi:10.1111/j.1461-0248.2007.01037.x
Dunne JA, Williams RJ, Martinez ND (2002) Network structure and biodiversity loss in food webs: robustness increases with connectance. Ecol Lett 5(4):558–567. doi:10.1046/j.1461-0248.2002.00354.x
Estrada E (2007) Food webs robustness to biodiversity loss: the roles of connectance, expansibility and degree distribution. J Theor Biol 244(2):296–307. doi:10.1016/j.jtbi.2006.08.002
Evans DM, Pocock MJO, Brooks J, Memmott J (2011) Seeds in farmland food-webs: resource importance, distribution and the impacts of farm management. Biol Conserv 144(12):2941–2950. doi:10.1016/j.biocon.2011.08.013
Fernandez-Palacios JM, de Nascimento L, Otto R, Delgado JD, Garcia-del-Rey E, Arevalo JR, Whittaker RJ (2011) A reconstruction of Palaeo-Macaronesia, with particular reference to the long-term biogeography of the Atlantic island laurel forests. J Biogeogr 38(2):226–246. doi:10.1111/j.1365-2699.2010.02427.x
Fortuna MA, Bascompte J (2006) Habitat loss and the structure of plant–animal mutualistic networks. Ecol Lett 9(3):278–283. doi:10.1111/j.1461-0248.2005.00868.x
Foster JT, Robinson SK (2007) Introduced birds and the fate of Hawaiian rainforests. Conserv Biol 21(5):1248–1257. doi:10.1111/j.1523-1739.2007.00781.x
Gibson R, Knott B, Eberlein T, Memmott J (2011) Sampling method influences the structure of plant–pollinator networks. Oikos 120(6):822–831
Global Invasive Species Database (2010) Global invasive species database. http://www.issg.org/database
González-Castro A, Traveset A, Nogales M (2012) Seed dispersal interactions in the Mediterranean region: contrasting patterns between islands and mainland. J Biogeogr. doi:10.1111/j.1365-2699.2012.02693.x
Gosper CR, Stansbury CD, Vivian-Smith G (2005) Seed dispersal of fleshy-fruited invasive plants by birds: contributing factors and management options. Divers Distrib 11(6):549–558. doi:10.1111/j.1366-9516.2005.00195.x
Heleno RH, Ceia RS, Ramos JA, Memmott J (2009) The effect of alien plants on insect abundance and biomass: a food web approach. Conserv Biol 23(2):410–419. doi:10.1111/j.1523-1739.2008.01129.x
Heleno RH, Lacerda I, Ramos JA, Memmott J (2010) Evaluation of restoration effectiveness: community response to the removal of alien plants. Ecol Appl 20(5):1191–1203. doi:10.1890/09-1384.1
Heleno RH, Ross G, Everard A, Ramos JA, Memmott J (2011) On the role of avian seed predators as seed dispersers. Ibis 153:199–203. doi:10.1111/j.1474-919X.2010.01088.x
Heleno R, Devoto M, Pocock M (2012a) Connectance of species interaction networks and conservation value: is it any good to be well connected? Ecol Ind 14(1):7–10. doi:10.1016/j.ecolind.2011.06.032
Heleno R, Olesen J, Nogales M, Vargas P, Traveset A (2012b) Seed dispersal networks in the Galápagos and the consequences of alien plant invasions. Proc R Soc B 280. doi:10.1098/rspb.2012.2112
Herrera CM (1995) Plant-vertebrate seed dispersal systems in the Mediterranean: ecological, evolutionary, and historical determinants. Annu Rev Ecol Syst 26:705–727. doi:10.1146/annurev.ecolsys.26.1.705
Jordano P (1987) Patterns of mutualistic interactions in pollination and seed dispersal—connectance, dependence asymmetries, and coevolution. Am Nat 129(5):657–677. doi:10.1086/284665
Kawakami K, Mizusawa L, Higuchi H (2009) Re-established mutualism in a seed-dispersal system consisting of native and introduced birds and plants on the Bonin Islands, Japan. Ecol Res 24(4):741–748. doi:10.1007/s11284-008-0543-8
Linnebjerg JF, Hansen DM, Bunbury N, Olesen JM (2010) Diet composition of the invasive red-whiskered bulbul Pycnonotus jocosus in Mauritius. J Trop Ecol 26(03):347–350. doi:10.1017/S0266467409990617
MacArthur R, Wilson E (1967) The theory of island biogeography. Princeton University Press, Princeton
Malmborg PK, Willson MF (1988) Foraging ecology of avian frugivores and some consequences for seed dispersal in an Illinois Woodlot. Condor 90(1):173–186. doi:10.2307/1368446
MEA (2005) Millennium Ecosystem Assessment—ecosystems and human well-being: a synthesis. Island Press, Washington, DC
Memmott J, Waser NM (2002) Integration of alien plants into a native flower–pollinator visitation web. Proc R Soc B 269(1508):2395–2399. doi:10.1098/rspb.2002.2174
Memmott J, Gibson R, Carvalheiro L, Henson K, Heleno R, Lopezaraiza M, Pearce S (2007) The conservation of ecological interactions. In: Stewart AA, New TR, Lewis OT (eds) Insect conservation biology. The Royal Entomological Society, London, pp 226–244
Milton SJ, Wilson JRU, Richardson DM, Seymour CL, Dean WRJ, Iponga DM, Proches S (2007) Invasive alien plants infiltrate bird-mediated shrub nucleation processes in arid savanna. J Ecol 95(4):648–661. doi:10.1111/j.1365-2745.2007.01247.x
Montesinos-Navarro A, Segarra-Moragues JG, Valiente-Banuet A, Verdú M (2012) The network structure of plant–arbuscular mycorrhizal fungi. New Phytol 194(2):536–547. doi:10.1111/j.1469-8137.2011.04045.x
Nathan R, Muller-Landau HC (2000) Spatial patterns of seed dispersal, their determinants and consequences for recruitment. Trends Ecol Evol 15(7):278–285. doi:10.1016/S0169-5347(00)01874-7
Olesen JM, Eskildsen LI, Venkatasamy S (2002) Invasion of pollination networks on oceanic islands: importance of invader complexes and endemic super generalists. Divers Distrib 8(3):181–192. doi:10.1046/j.1472-4642.2002.00148.x
Padrón B, Traveset A, Biedenweg T, Díaz 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
Padrón B, Nogales M, Traveset A, Vilà M, Martinez-Abrain A, Padilla DP, Marrero P (2011) Integration of invasive Opuntia spp. by native and alien seed dispersers in the Mediterranean area and the Canary Islands. Biol Invasions 13(4):831–844. doi:10.1007/s10530-010-9872-y
R Development Core Team (2010) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Ramos JA (1996) Introduction of exotic tree species as a threat to the Azores bullfinch population. J Appl Ecol 33(4):710–722. doi:10.2307/2404942
Renne IJ, Barrow WC, Randall LAJ, Bridges WC (2002) Generalized avian dispersal syndrome contributes to Chinese tallow tree (Sapium sebiferum, Euphorbiaceae) invasiveness. Divers Distrib 8(5):285–295. doi:10.1046/j.1472-4642.2002.00150.x
Saracco JF, Collazo JA, Groom MJ, Carlo TA (2005) Crop size and fruit neighborhood effects on bird visitation to fruiting Schefflera morototoni trees in Puerto Rico. Biotropica 37(1):81–87
Schaeffer H (2002) Flora of the Azores a field guide. Margraf Verlag, Weikersheim
Schupp EW, Jordano P, Gómez JM (2010) Seed dispersal effectiveness revisited: a conceptual review. New Phytol 188:333–353. doi:10.1111/j.1469-8137.2010.03402.x
Silva LD (2001) Plantas vasculares invasoras no Arquipélago dos Açores - PhD thesis. University of the Azores, Ponta Delgada
Silva IA, Figueiredo RAd, Matos DMdS (2008) Feeding visit time of fruit-eating birds in Cerrado plants revisiting the predation risk model. Rev Bras Zool 25(4):682–688
Silva L, Moura M, Schaefer H, Rumsey F, Dias EF (2010) List of vascular plants (Tracheobionta). In: Borges PAV, Costa A, Cunha R et al (eds) A list of the terrestrial and marine biota from the Azores. Princípia, Cascais, pp 131–155
SPEA (2005) Plano de gestão da ZPE Pico da Vara/Ribeira do Guilherme
Stansbury CD (2001) Dispersal of the environmental weed Bridal Creeper, Asparagus asparagoides, by Silvereyes, Zosterops lateralis, in south-western Australia. Emu 101(1):39–45. doi:10.1071/mu00069
Thébault E, Fontaine C (2010) Stability of ecological communities and the architecture of mutualistic and trophic networks. Science 329:853–856. doi:10.1126/science.1188321
Traveset A, Richardson DM (2011) Mutualisms: key drivers of invasions… key casualties of invasions. Fifty years of invasion ecology: the legacy of Charles Elton. Wiley-Blackwell, Oxford
Tutin TG (1953) The vegetation of the Azores. J Ecol 41(1):53–61
Vilà M, Bartomeus I, Dietzsch AC, Petanidou T, Steffan-Dewenter I, Stout JC, Tscheulin T (2009) Invasive plant integration into native plant–pollinator networks across Europe. Proc R Soc B 276(1674):3887–3893. doi:10.1098/rspb.2009.1076
Vitousek PM, D’Antonio CM, Loope LL, Westbrooks R (1996) Biological invasions as global environmental change. Am Sci 84(5):468–478
Warren PH (1994) Making connections in food webs. Trends Ecol Evol 9(4):136–141. doi:10.1016/0169-5347(94)90178-3
Whittaker RJ, Fernández-Palacios JM (2007) Island biogeography: ecology, evolution, and conservation. Oxford University Press, Oxford
Williams PA (2006) The role of blackbirds (Turdus merula) in weed invasion in New Zealand. N Z J Ecol 30(2):285–291
Williams PA, Karl BJ (1996) Fleshy fruits of indigenous and adventive plants in the diet of birds in forest remnants, Nelson, New Zealand. N Z J Ecol 20(2):127–145
Wolfram Research (1999) Mathematica, version 6.0. Champaign
Acknowledgments
We thank the LIFE-Priolo team, particularly Ricardo Ceia, Hugo Sampaio, Carlos Silva and Sandra Parejo for all the logistic support in the field, Márcia Santos, Bronwen Lester and Catarina Heleno for help during fieldwork, and Rachel Gibson and Mariano Devoto for sharing R code.
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Heleno, R.H., Ramos, J.A. & Memmott, J. Integration of exotic seeds into an Azorean seed dispersal network. Biol Invasions 15, 1143–1154 (2013). https://doi.org/10.1007/s10530-012-0357-z
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DOI: https://doi.org/10.1007/s10530-012-0357-z