Hostname: page-component-cd9895bd7-fscjk Total loading time: 0 Render date: 2024-12-27T23:28:07.929Z Has data issue: false hasContentIssue false
  • English
  • Français

Structure of mutualistic ant–treehopper interactions in the Brazilian Atlantic Forest

Published online by Cambridge University Press:  10 May 2016

Yve Eligiêr Alves Gadelha ,
Wesley Dáttilo ,
Olivia Evangelista  and
Benedito Cortês Lopes
Yve Eligiêr Alves Gadelha*
Affiliation:
Programa de Pós-Graduação em Ecologia, Universidade Federal de Santa Catarina, Florianópolis, Brazil
Wesley Dáttilo
Affiliation:
Red de Ecoetología, Instituto de Ecología A.C., Xalapa, Veracruz, Mexico
Olivia Evangelista
Affiliation:
Museu de Zoologia, Universidade de São Paulo, São Paulo, Brazil
Benedito Cortês Lopes
Affiliation:
Departamento de Ecologia e Zoologia, Centro de Ciências Biológicas, Universidade Federal de Santa Catarina, Florianópolis, Brazil
*
1Corresponding author. Email: yvegadelha@gmail.com
Get access Rights & Permissions [Opens in a new window]

Abstract:

Ant–treehopper mutualisms are centred on the availability of honeydew, a sugary fluid offered by treehoppers to attract ants, which respond by defending their hosts against predators and parasitoids. However, due to differences in the treehopper social behaviour (i.e. the amount of food resource available) ants can monopolize treehopper aggregations in many ways. Here we evaluated the topological structure of quantitative ant–treehopper interaction networks in three Brazilian Atlantic Forest localities. Moreover, we specifically investigated the role of ant recruitment strategy and treehopper behaviour in the structure of these networks. For this, we sampled ant–treehopper interactions along representative transects (6 km per site) within each studied site and recorded the mean number of individuals of treehopper and ant species. We found that independent of variation in environmental factors among study sites, ant–treehopper networks were highly compartmentalized (Mean ± SD: Q = 0.34 ± 0.1) when compared with null models, and exhibit low connectance (C = 0.18 ± 0.01) and specialization (H2’ = 0.36 ± 0.08) values. In addition, we also observed that larger aggregations of treehoppers interacted with a higher number of ant species and ants that were locally dominant and showed massive recruitment interacted with a larger number of treehopper species. In summary, our results illustrate the importance of foraging strategies in shaping ecological interactions in tropical environments.

Keywords

ant–treehopper interactionecological networksfacultative mutualismMembracidaeweighted nestedness
Type
Research Article
Information
Journal of Tropical Ecology , Volume 32 , Issue 3 , May 2016 , pp. 250 - 259
Copyright
Copyright © Cambridge University Press 2016 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

LITERATURE CITED

ALMEIDA-NETO, M. & ULRICH, W. 2011. A straightforward computational approach for measuring nestedness using quantitative matrices. Environmental Modelling and Software 26:173–178.Google Scholar
ALVARES, C. A., STAPE, J. L., SENTELHAS, P. C., GONÇALVES, J. L. M. & SPAROVEK, G. 2013. Köppen's climate classification map for Brazil. Meteorologische Zeitschrift: Fast Track Article:1–18.Google Scholar
BARRIGA, P. O., DORMANN, C. F., GBUR, E. E. & SAGERS, C. R. 2015. Community structure and ecological specialization in plant-ant interactions. Journal of Tropical Ecology 31:325–334.Google Scholar
BASCOMPTE, J., JORDANO, P., MELIAN, C. J. & OLESEN, J.M. 2003. The nested assembly of plant-animal mutualistic networks. Proceedings of the National Academy of Sciences USA 100:9383–9387.Google Scholar
BASCOMPTE, J., JORDANO, P. & OLESEN, J. M. 2006. Asymmetric coevolutionary networks facilitate biodiversity maintenance. Science 312:431–433.CrossRefGoogle ScholarPubMed
BATAGELJ, V. & MRVAR, A. 1998. Pajek – a program for large network analysis. Connections 21:47–57.Google Scholar
BENÍTEZ-MALVIDO, J. & DÁTTILO, W. 2015. Interaction intimacy of pathogens and herbivores with their plant hosts influences the topological structure of ecological networks in different ways. American Journal of Botany 102:1–8.Google Scholar
BELLAY, S., OLIVEIRA, E. F., ALMEIDA-NETO, M., ABDALLAH, V. D., AZEVEDO, R. K., TAKEMOTO, R. M. & LUQUE, J. L. 2015. The patterns of organisation and structure of interactions in a fish-parasite network of a Neotropical river. International Journal for Parasitology 45:549–557.Google Scholar
BLIGHT, O., ORGEAS, J., TORRE, F. & PROVOST, E. 2014. Competitive dominance in the organisation of Mediterranean ant communities. Ecological Entomology 39:595–602.Google Scholar
BLÜTHGEN, N. & FIEDLER, K. 2004. Competition for composition: lessons from nectar-feeding ant communities. Ecology 85:1479–1485.Google Scholar
BLÜTHGEN, N., VERHAAGH, M., GOITIA, W., JAFFE, K., MORAWETZ, W. & BARTHLOTT, W. 2000. How plants shape the ant community in the Amazonian rainforest canopy: the key role of extrafloral nectaries and homopteran honeydew. Oecologia 125:229–240.CrossRefGoogle ScholarPubMed
BLÜTHGEN, N., MENZEL, F. & BLÜTHGEN, N. 2006. Measuring specialization in species interaction networks. BMC Ecology 6 (9):1–12.Google Scholar
BLÜTHGEN, N., MENZEL, F., HOVESTADT, T., FIALA, B. & BLÜTHGEN, N. 2007. Specialization, constraints, and conflicting interests in mutualistic networks. Current Biology 17:341–346.Google Scholar
CLEMENTE, M. A., LANGE, D., DEL-CLARO, K., PREZOTO, F., CAMPOS, N. R. & BARBOSA, B. C. 2012. Flower-visiting social wasps and plants interaction: network pattern and environmental complexity. Psyche 2012:478431.Google Scholar
CORSO, G. & BRITTON, N. F. 2014. Comparisons and contrasts between asymmetry and nestedness in interacting ecological networks. Open Journal of Ecology 4:653–661.Google Scholar
DÁTTILO, W., RICO-GRAY, V., RODRIGUES, D. J. & IZZO, T. J. 2013a. Soil and vegetation features determine the nested pattern of ant-plant networks in a tropical rainforest. Ecological Entomology 38:374–380.Google Scholar
DÁTTILO, W., GUIMARÃES, P. R. & IZZO, T. J. 2013b. Spatial structure of ant-plant mutualistic networks. Oikos 122:1643–1648.CrossRefGoogle Scholar
DÁTTILO, W., SÁNCHEZ-GALVÁN, I., LANGE, D., DEL-CLARO, K., & RICO-GRAY, V. 2014a. Importance of interaction frequency in analysis of ant-plant networks in tropical environments. Journal of Tropical Ecology 30:165–168.Google Scholar
DÁTTILO, W., DÍAZ-CASTELAZO, C. & RICO-GRAY, V. 2014b. Ant dominance hierarchy determines the nested pattern in ant-plant networks. Biological Journal of the Linnean Society 113:405–414.CrossRefGoogle Scholar
DEL-CLARO, K. & OLIVEIRA, P. S. 1999. Ant-homoptera interactions in a neotropical savanna: the honeydew-producing treehopper Guayaquila xiphias (Membracidae) and is associated ant fauna on Didymopanax vinosum (Araliaceae). Biotropica 31:135–144.Google Scholar
DORMANN, C. F. & STRAUSS, R. 2014. A method for detecting modules in quantitative bipartite networks. Methods in Ecology and Evolution 5 (1):90–98.CrossRefGoogle Scholar
DORMANN, C. F., GRUBER, B. & FRUND, J. 2008. Introducing the bipartite package: analyzing ecological networks. R News 8:8–11.Google Scholar
FAGUNDES, R., RIBEIRO, S. P. & DEL-CLARO, K. 2013. Tending-ants increase survivorship and reproductive success of Calloconophora pugionata Dietrich (Hemiptera, Membracidae), a trophobiont herbivore of Myrcia obovata O. Berg (Myrtales, Myrtaceae). Sociobiology 60:11–19.Google Scholar
FENG, W. & TAKEMOTO, K. 2014. Heterogeneity in ecological mutualistic networks dominantly determines community stability. Scientific Reports 4 (5912):1–11.Google Scholar
FERNÁNDEZ, F. 2003. Subfamília Myrmicinae. Pp. 307–330 in Fernández, P. (ed.). Introducción a las Hormigas de la Región Neotropical. Instituto de Investigación de Recursos Biológicos Alexander von Humboldt, Bogotá.Google Scholar
JAMES, A., PITCHFORD, J. W. & PLANK, M. J. 2012. Disentangling nestedness from models of ecological complexity. Nature 487:227–230.Google Scholar
KAMINSKI, L. A., FREITAS, A. V. L. & OLIVEIRA, P. S. 2010. Interaction between mutualisms: ant-tended butterflies exploit enemy-free space provided by ant-treehopper associations. American Naturalist 176:322–334.CrossRefGoogle ScholarPubMed
KATAYAMA, N., TSUCHIDA, T., HOJO, M. K. & OHGUSHI, T. 2013. Aphid genotype determines intensity of ant attendance: do endosymbionts and honeydew composition matter? Annals of the Entomological Society of America 106:761–770.Google Scholar
LANGE, D. & DEL-CLARO, K. 2014. Ant-plant interaction in a tropical savanna: may the network structure vary over time and influence on the outcomes of associations? PLoS ONE 9:1–10.CrossRefGoogle Scholar
LANGE, D., DÁTTILO, W. & DEL-CLARO, K. 2013. Influence of extrafloral nectary phenology on ant-plant mutualistic networks in a neotropical savanna. Ecological Entomology 38:463–469.Google Scholar
LIN, C. P. 2006. Social behaviour and life history of membracine treehoppers. Journal of Natural History 40:1887–1907.Google Scholar
LONGINO, J. T. 2003. The Crematogaster (Hymenoptera, Formicidae, Myrmicinae) of Costa Rica. Zootaxa 151:1–150.CrossRefGoogle Scholar
MELLO, M. A. R., BEZERRA, E. L. S. & MACHADO, I. C. 2013. Functional roles of Centridini oil bees and Malpighiaceae oil flowers in biome-wide pollination networks. Biotropica 45:45–53.Google Scholar
MORALES, M. A. & BEAL, A. L. H. 2006. Effects of host plant quality and ant tending for treehopper Publilia concave. Annals of the Entomological Society of America 99:545–552.Google Scholar
MOREIRA, V. S. S. & DEL-CLARO, K. 2005. The outcomes of an ant-treehopper association on Solanum lycocarpum St. Hill: increased membracid fecundity and reduced damage by chewing herbivores. Neotropical Entomology 34:881–887.Google Scholar
NAUMANN, K. 1994. An occurrence of two exotic ant (Formicidae) species in British Columbia. Journal of the Entomological Society of British Columbia 91:69–70.Google Scholar
PANDOLFO, C., BRAGA, H. J., SILVA, V. P., MASSIGNAM, A. M., PEREIRA, E. S., THOMÉ, V. M. R. & VALCI, F. V. 2002. Atlas climatológico digital do Estado de Santa Catarina. Epagri, Florianópolis, Brasil.Google Scholar
PASSMORE, H. A., BRUNA, E. M., HEREDIA, S. M. & VASCONCELOS, H. L. 2012. Resilient networks of ant-plant mutualisms in Amazonian forest fragments. PLoS ONE 7:1–8.CrossRefGoogle ScholarPubMed
PIGOZZO, C. M. & VIANA, B. F. 2010. Estrutura da rede de interações ente flores e abelhas em ambiente de Caatinga. Oecologia Australis 14:100–114.Google Scholar
RICO-GRAY, V. 1993. Use of plant-derived food resources by ants in the dry tropical lowlands of coastal Veracruz, Mexico. Biotropica 25:301–315.Google Scholar
RICO-GRAY, V., DIÁZ-CASTELAZO, C., RAMÍREZ-HERNÁNDEZ, A., GUIMARÃES, P. R. & HOLLAND, J. N. 2012. Abiotic factors shape temporal variation in the structure of an ant-plant network. Arthropod–Plant Interactions 6:289–295.Google Scholar
ROBINSON, K. M., HAUZY, C., LOEUILLE, N. & ALBRECTSEN, B. R. 2015. Relative impacts of environmental variation and evolutionary history on the nestedness and modularity of tree-herbivore networks. Ecology and Evolution 5 (14):2898–2915.Google Scholar
RODERJAN, C. T. & KUNIYOSHI, Y. S. 1988. Macrozoneamento florístico da Área de Proteção Ambiental de Guaraqueçaba. FUPEF, Curitiba, Brazil.Google Scholar
ROHR, R. P., SAAVEDRA, S. & BASCOMPTE, J. 2014. On the structural stability of mutualistic systems. Science 345:416–426.Google Scholar
SANTOS, G. M. M., AGUIAR, C. M. L. & MELLO, M. A. R. 2010. Flower-visiting guild associated with the Caatinga flora: trophic interaction networks formed by social bees and social wasps with plants. Apidologie 41:466–475.Google Scholar
SANTOS, G. M. M., DÁTTILO, W. & PRESLEY, S. J. 2014. The seasonal dynamic of ant-flower networks in a semi-arid tropical environment. Ecological Entomology 39:674–683.Google Scholar
SCHOEREDER, J. H., SOBRINHO, T. G., MADUREIRA, M. S., RIBAS, C. R. & OLIVEIRA, P. S. 2010. The arboreal ant community visiting extrafloral nectaries in the Neotropical cerrado savanna. Terrestrial Arthropod Reviews 3:3–27.Google Scholar
STAAB, M., BLÜTHGEN, N. & KLEIN, A. M. 2014. Tree diversity alters the structure of a tri-trophic network in a biodiversity experiment. Oikos 124:827–834.Google Scholar
STANICZENKO, P. P. A., KOPP, J. C. & ALLESINA, S. 2013. The ghost of nestedness in ecological networks. Nature Communications 4:1390–1396.Google Scholar
STRONA, G. & VEECH, J. A. 2015. A new measure of ecological network structure based on node overlap and segregation. Methods in Ecology and Evolution 6:907–915.Google Scholar
SUWEIS, S., SIMINI, F., BANAVAR, J. R. & MARITAN, A. 2013. Emergence of structural and dynamical properties of ecological mutualistic networks. Nature 500:449–452.Google Scholar
VÁZQUEZ, D. P., MELIÁN, C. J., WILLIAMS, N. M., BLÜTHGEN, N., KRASNOV, B. R. & POULIN, R. 2007. Species abundance and asymmetric interaction strength in ecological networks. Oikos 116:120–127.Google Scholar
VIZENTIN-BUGONI, J., MARUYAMA, P. K., DEBASTIANI, V. J., DUARTE, L. S., DALSGAARD, B. & SAZIMA, M. 2016. Influences of sampling effort on detected patterns and structuring processes of a Neotropical plant-hummingbird network. Journal of Animal Ecology 85:262–272.CrossRefGoogle ScholarPubMed
WETTERER, J. K. & PORTER, S. D. 2003. The little fire ant, Wasmannia auropunctata: distribution, impact and control. Sociobiology 41:1–41.Google Scholar
WOOD, T. K. 1993. Diversity in the New World Membracidae. Annual Review of Entomology 38:409–435.Google Scholar