Comparing the Structure and Robustness of Passifloraceae - Floral Visitor and True Pollinator Networks in a Lowland Atlantic Forest

Authors

  • Cristine Rodrigues Benevides Universidade Estadual do Norte Fluminense Darcy Ribeiro
  • Darren M Evans University of Hull
  • Maria Cristina Gaglianone Universidade Estadual do Norte Fluminense Darcy Ribeiro

DOI:

https://doi.org/10.13102/sociobiology.v60i3.295-305

Keywords:

Floral syndromes, pollination ecology, plant-pollinator network structure, crop pollinators

Abstract

We investigated the plant-pollinator interactions of Passifloraceae occurring in fragments of lowland semi-deciduous Atlantic forest. We described floral biology, pollination syndromes and the pollinators of Passiflora alata, Passiflora kermesina, Passiflora suberosa, Passiflora malacophylla and Mitostemma glaziovii. We examined the robustness of the interaction networks to species loss, a plausible scenario resulting from forest fragmentation. The effects of pollination syndrome (flower size) on network robustness was also examined. Passiflora alata, P. malacophylla and P. suberosa were pollinated by bees of different corporal sizes. P. kermesina and M. glaziovii presented the highest diversity of visitors and were pollinated mainly by hummingbirds and butterflies, respectively. Through the analysis of the networks we differentiate the structures of the flower-visitor network with the ‘true’ plant-pollinator network. The robustness of the flower-visitor network to animal loss was generally high, but it declined when only true pollinators were included in the network. The sequential loss of plants from the flower-visitor network resulted in low robustness: the loss of key plants could have significant cascading effects on the animals feeding on them within the forest fragment. Future studies should consider the interactions between all flowering plants and animals in this habitat in order to guide conservation and management plans for these forest fragments.

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References

Aguiar, W.M. & Gaglianone, M.C. (2008). Comunidade de abelhas Euglossina (Hymenoptera: Apidae) em remanescentes de mata estacional semidecidual sobre tabuleiro no estado do Rio de Janeiro. Neotrop. Entomol., 37: 118-125.

Almeida-Neto, M. Guimarães, P.R., Guimarães, P.R. Jr, Loyola R.D.,Ulrich, W. (2008). A consistent metric for nestedness analysis in ecological systems: reconciling concept and quantification. Oikos, 117: 1227-1239.

Bascompte, J., Jordano, P., Melián, C.J. & Olesen, J.M. (2003). The nested assembly of plan-animal mutualistic networks. Proc. Natl. Acad. Sci. USA, 100: 9383-9387.

Benevides, C.R., Gaglianone, M.C. & Hoffmann, M. (2009).Visitantes Florais do Maracujá-amarelo (Passiflora edulis f. flavicarpa Deg. Passifloraceae) em Áreas de Cultivo com Diferentes Proximidades a Fragmentos Florestais na Região Norte Fluminense, RJ. Rev. Bras. Entomol., 53: 415-421.

Benson, W.W., Brown, J.R. & Gilbert, L.E. (1976). Coevolution of plants and herbivores: passion flower butterflies. Evolution, 29: 650-680.

Bernacci, L.C., Cervi, A.C., Milward-de-Azevedo, M.A., Nunes, T.S., Imig, D.C., Mezzonato, A.C. (2013). Passifloraceae in Lista de Espécies da Flora do Brasil. Jardim Botânico do Rio de Janeiro. (http://floradobrasil.jbrj.gov.br/jabot/floradobrasil/FB12505).

Bernardino, A.S. & Gaglianone, M.C. (2013). Comparisons in nesting biology of two sympatric carpenter bee species (Apidae: Xylocopini), J. Nat. Hist., 47: 1481-1499. doi :10.1080/00222933.2012.763054.

Biesmeijer, J. C., Roberts, S.P.M., Reemer, M., Ohlemuller, R., Edwards, M., Peeters, T., Schaffer, A.P., Potts, S.G., Kleukers, R., Thomas, C.D., Settele, J., Kunin, W.E. (2006). Parallel declines in pollinators and insect-pollinated plants in Britain and the Netherlands. Science, 313(5785): 351-354.

Burgos, E., Ceva, H. R., Perazzo P.J., Devoto M., Medan, D. Zimmermann, M., & Delbue, A.M. (2007). Why nestedness in mutualistic networks? J. Theor. Biol., 249: 307-313.

Buzato, S. & Franco, A.L.M. (1992). Tetrastylis ovalis: a second case of bat-pollinated passsion flower (Passifloraceae). Plant Syst. Evol., 181: 261-267.

Chamberlain, S.A. & Holland, J.N. (2009). Body size predicts degree in ant-plant mutualistic networks. Funct. Ecol., 23: 196-202.

Dafni, A. (1992). Pollination Ecology: a practical approach. New York: Oxford University Press.

Danieli-Silva, A., Souza J.M.T., Donatti, A.J., Campos, R.P., Vicente-Silva.J, Freitas L. & Varassin, I.G. (2012). Do pollination syndromes cause modularity and predict interactions in a pollination network in tropical high-altitude grasslands? Oikos, 121: 35-43.

Dunne, J.A., Williams, R.J. & Martinez, N.D. (2002). Network structure and biodiversity loss in food webs: robustness increases with connectance. Ecol. Lett., 5: 558-567.

Faegri, K. & Pijl, L.V.D. (1979).The Principles of Pollination Ecology.Third Revised Edition. London: Pergamon Press.

Fischer, E. & Leal, I.R. (2006). Effect of nectar secretion rate on pollination success of Passiflora coccinea (Passifloraceae) in the Central Amazon. Braz. J. Biol., 66: 747-754.

Gaglianone, M.C. (2006). Centridini em remanescentes de Mata Atlântica: diversidade e interações com flores. In: VII Encontro sobre Abelhas, 2006, Ribeirão Preto. Anais do VII Encontro sobre abelhas, 1, 6-11.

Gaglianone, M.C., Rocha, H.H.S., Benevides, C.R., Junqueira C.N. & Augusto, S.C. (2010). Importância de Centridini (Apidae) na polinização de plantas de interesse agrícola: o maracujá-doce (Passiflora alata Curtis) como estudo de caso na região sudeste do Brasil. Oecololgia Australis, 14: 152-164.

Gentry, A.H. (1974). Flowering phenology and diversity in tropical Bignoniaceae. Biotropica, 6: 64-68.

Hagen, M., Kissling, W.D., Rasmussen, C., De Aguiar, M.A.M., Brown, L.E., Carstensen, D.W. et al. (2012). Biodiversity, species interactions and ecological networks in a fragmented world. Adv. Ecol. Res., 46: 89-210.

Hingston, A.B. & McQuillan, P.B. (2000). Are pollination syndromes useful predictors of floral visitors in Tasmania? Austral Ecol, 25: 600-609.

Janzen, D.H. (1971). Euglossine bees as long-distance pollinators of tropical plants. Science, 171: 203-205.

Jordano, P., Bascompte, J. & Olesen, J.M. (2003). Invariant properties in coevolutionary networks of plant-animal interactions. Ecol. Lett., 6: 69-81.

Kaiser-Bunbury, C.N., Muff, S., Memmott, J., Muller, C.B. & Caflisch, A. (2010). The robustness of pollination networks to the loss of species and interactions: a quantitative approach incorporating pollinator behaviour. Ecol. Lett., 13: 442-452.

Koschnitzke, C. & Sazima, M. (1997). Biologia floral de cinco espécies de Passiflora L. (Passifloraceae) em mata semidecídua. Rev. Bras. Bot., 20: 19-126.

Magurran, A.E. (1988). Ecological diversity and its measurement. Princeton University Press. Princeton.

Memmott, J., Craze, P.G., Waser, N.M. & Price, M.V. (2007). Global warming and the disruption of plant-pollinator interactions. Ecol. Lett., 10: 710-717.

Memmott, J., Waser, N.M. & Price, M.V. (2004). Tolerance of pollination networks to species extinctions. Proc. Biol. Sci., 271: 2605-2611.

Montoya, J.M., Pimm, S.L. & Sole, R.V. (2006). Ecological networks and their fragility. Nature, 442: 259-264.

Morellato, PL.P.C.,Talora, D.T., Takahasi, A., Bencke, C.C., Romera E.C. & Zipparro, V.B. (2000). Phenology of Atlantic Rain Forest Trees: A Comparative Study. Biotropica, 32: 811-823.

Ollerton, J., Alarco, R., Waser, N.M., Price, M.V., Watts, S., Cranmer, L., Hingston, A., Peter, C.I. & Rotenberry, J. (2009). A global test of the pollination syndrome hypothesis. Ann. Bot.-London, 103: 1471-1480.

Pocock, M.J.O., Evans, D.M. & Memmott, J. (2012). The robustness and restoration of a network of ecological networks. Science, 335: 973-977.

Ratchcke, B. & Lacey, E.P. (1985). Phenological patterns of terrestrial plants. Annu. Rev. Ecol. Syst., 16: 179-214.

Richards, A.J. (1986). Plant breeding systems. Allen & Unwin, London.

Rizzini, C. T. (1979). Tratado de Fitogeografia do Brasil - aspectos sociológicos e florísticos. v.2. Editora HUCITEC / EDUSP. São Paulo, SP.

Santos, G.M.M., Aguiar, C.M.L., Genini, J., Martins, C.F., Zanella, F.C.V, Mello, M.A.R. (2012). Invasive Africanized honeybees change the structure of native pollination networks in Brazil. Biol. Invasions, 14: 2369-2378. doi 10.1007/s10530-012-0235-8.

Sazima, M. & Sazima, I. (1978). Bat pollination of the Passion flower, Passiflora mucronata, in Southeastern Brazil. Biotropica, 10: 100-109.

Silva, G.C. & Nascimento, M.T. (2001). Fitossociologia de um remanescente de mata sobre tabuleiro no Norte do Estado do Rio de Janeiro (Mata do Carvão). Rev. Bras. Bot., 24, 51-62.

Souza, V.C. & Lorenzi, H. (2005). Botânica sistemática: Guia ilustrado para identificação das famílias de Angiospermas da flora brasileira, baseado em APG II. Plantarum, Nova Odessa.

Staniczenko, P.P.A., Lewis, O.T., Jones, N.S. & Reed-Tsochas, F. (2010). Structural dynamics and robustness of food webs. Ecol. Lett., 13: 891-899.

Tylianakis, J.M., Didham, R.K., Bascompte, J. & Wardle, D.A. (2008). Global change and species interactions in terrestrial ecosystems. Ecol. Lett., 11: 1351-1363.

Varassin, I.G. & Silva, A.G. (1999). A melitofilia em Passiflora alata Dryander (Passifloraceae), em Vegetação de Restinga. Rodriguésia, 50(76/77): 5-17.

Varassin, I. G., Trigo, J. R. & Sazima, M. (2001).The role of nectar production, flower pigments and odour in the pollination of four species of Passiflora (Passifloraceae) in south- eastern Brazil. Bot. J. Linn. Soc., 136: 139-152.

Villela, D.M., Nascimento, M.T., Aragão, L.E.O.C., Da Gama, D.M. (2006). Effect of selective logging on forest structure and nutrient cycling in a seasonally dry Brazilian Atlantic forest. J. Biogeogr., 33: 506-516.

Vitta, F.A. (1997). Passiflora loefgrenii (Passifloraceae), a New Species in Subgenus Passiflora from the Brazilian Atlantic Rain forest. Novon, 7: 210-212.

Vogel, S. (1983). Ecophysiology of zoophilic pollination. InLage, O.L., Nobel, P.S., Osmond, C.B. & Ziegler, H. (Eds.). Physiological Plant Ecology. III. Encyclopedia of Plant Physiology. (pp. 559-624) Heidelburg: Springer-Verlag.

Waddington, K.D. (1983). Foraging behavior of pollinators. Pollination Biol., 9: 213-223.

Yamamoto, M., Silva, C.I., Augusto, S.C., Barbosa, A.A.A.& Oliveira, P.E. (2012). The role of bee diversity in pollination and fruit set of yellow passion fruit (Passiflora edulis forma flavicarpa, Passifloraceae) crop in Central Brazil. Apidologie, 43: 515-526, doi: 10.1007/s13592-012-0120-6

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Published

2013-11-06

How to Cite

Benevides, C. R., Evans, D. M., & Gaglianone, M. C. (2013). Comparing the Structure and Robustness of Passifloraceae - Floral Visitor and True Pollinator Networks in a Lowland Atlantic Forest. Sociobiology, 60(3), 295–305. https://doi.org/10.13102/sociobiology.v60i3.295-305

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Section

Research Article - Bees