Skip to main content
SpringerLink
Log in

Foliage-dwelling ants in a neotropical savanna: effects of plant and insect exudates on ant communities

  • Original Paper
  • Published:
Arthropod-Plant Interactions Aims and scope Submit manuscript

Abstract

Ant dominance in tropical ecosystems can be explained by a capacity to exploit liquid foods such as extrafloral nectaries (EFNs) and secretions from honeydew-producing hemipterans (HPHs). Such nutritious exudates may determine ant distribution in space and shape specialization in ant–plant interactions. We provide a first assessment of how EFNs and HPHs mediate the structure of ant assemblages, ant visitation intensity, and characteristics of ant–plant interaction networks across space in Brazilian “cerrado” savanna. We used arboreal pitfall traps to sample visiting ants in four cerrado localities and recorded the presence of lepidopteran larvae to determine their possible response to ant visitation. Ant species composition and richness did not differ regardless of the presence of liquid rewards on plants, and most network patterns did not show consistent differences. However, in two of the four sites, ant densities were higher on plants with HPHs or EFNs due to increased activity by Camponotus and Pseudomyrmex ants. At these two sites, plants with liquid food sources had a more specific ant assemblage (higher specialization d′) than did plants without resources, and caterpillars were more frequently found on plants with fewer workers of Camponotus and Pseudomyrmex. Plants with HPHs had increased ant visitation and accumulated more ant species than did plants with EFNs or without liquid foods. Ant response to such food sources may thus depend on local conditions and identity of ant species, and may determine how ant assemblages are structured. Results highlight how different patterns of ant visitation to liquid resources can produce distinctive effects on herbivore infestation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Almeida-Neto M, Ulrich W (2011) A straightforward computational approach for measuring nestedness using quantitative matrices. Environ Model Softw 26:173–178. doi:10.1016/j.envsoft.2010.08.003

    Article  Google Scholar 

  • Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate—a practical and powerful approach to multiple testing. J R Stat Soc B 57:289–300

    Google Scholar 

  • Blüthgen N (2010) Why network analysis is often disconnected from community ecology: a critique and an ecologist’s guide. Basic Appl Ecol 11:185–195. doi:10.1016/j.baae.2010.01.001

    Article  Google Scholar 

  • Blüthgen N, Feldhaar H (2010) Food and shelter: how resources influence ant ecology. In: Lach L, Parr C, Abbott KL (eds) Ant ecology. Oxford University Press, New York, pp 115–136

    Google Scholar 

  • Blüthgen N, Fiedler K (2004) Preferences for sugars and amino acids and their conditionality in a diverse nectar-feeding ant community. J Anim Ecol 73:155–166

    Article  Google Scholar 

  • Blüthgen N, Stork NE (2007) Ant mosaics in a tropical rainforest in Australia and elsewhere: a critical review. Austral Ecol 32:93–104. doi:10.1111/j.1442-9993.2007.01744.x

    Article  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

    Article  PubMed  Google Scholar 

  • Blüthgen N, Stork NE, Fiedler K (2004) Bottom-up control and co-occurrence in complex communities: honeydew and nectar determine a rainforest ant mosaic. Oikos 106:344–358. doi:10.1111/j.0030-1299.2004.12687.x

    Article  Google Scholar 

  • Blüthgen N, Menzel F, Blüthgen N (2006) Measuring specialization in species interaction networks. BMC Ecol 6:9. doi:10.1186/1472-6785-6-9

    Article  PubMed  PubMed Central  Google Scholar 

  • Blüthgen N, Menzel F, Hovestadt T, Fiala B, Bluthgen N (2007) Specialization, constraints, and conflicting interests in mutualistic networks. Curr Biol 17:341–346

    Article  PubMed  Google Scholar 

  • Campos R, Camacho G (2014) Ant–plant interactions: the importance of extrafloral nectaries versus hemipteran honeydew on plant defense against herbivores. Arthropod Plant Interact. doi:10.1007/s11829-014-9338-8

    Google Scholar 

  • Chamberlain SA, Holland JN (2009) Quantitative synthesis of context dependency in ant–plant protection mutualisms. Ecology 90:2384–2392. doi:10.1890/08-1490.1

    Article  PubMed  Google Scholar 

  • Dáttilo W, Guimaraes PR, Izzo TJ (2013) Spatial structure of ant–plant mutualistic networks. Oikos 122:1643–1648. doi:10.1111/j.1600-0706.2013.00562.x

    Article  Google Scholar 

  • Dáttilo W, Marquitti FMD, Guimarães PR, Izzo TJ (2014) The structure of ant–plant ecological networks: is abundance enough? Ecology 95:475–485. doi:10.1890/12-1647.1

    Article  PubMed  Google Scholar 

  • Davidson DW (1997) The role of resource imbalances in the evolutionary ecology of tropical arboreal ants. Biol J Linn Soc 61:153–181

    Article  Google Scholar 

  • Davidson DW, Cook SC, Snelling RR, Chua TH (2003) Explaining the abundance of ants in lowland tropical rainforest canopies. Science 300:969–972

    Article  CAS  PubMed  Google Scholar 

  • Del-Claro K, Oliveira PS (1999) Ant-Homoptera interactions in a neotropical savanna: the honeydew-producing treehopper, Guayaquila xiphias (Membracidae), and its associated ant fauna on Didymopanax vinosum (Araliaceae). Biotropica 31:135–144. doi:10.1111/j.1744-7429.1999.tb00124.x

    Google Scholar 

  • Del-Claro K, Oliveira PS (2000) Conditional outcomes in a neotropical treehopper-ant association: temporal and species-specific variation in ant protection and homopteran fecundity. Oecologia 124:156–165

    Article  Google Scholar 

  • Diaz-Castelazo C, Rico-Gray V, Oliveira PS, Cuautle M (2004) Extrafloral nectary-mediated ant–plant interactions in the coastal vegetation of Veracruz, Mexico: richness, occurrence, seasonality, and ant foraging patterns. Ecoscience 11:472–481

    Google Scholar 

  • Díaz-Castelazo C, Guimarães PR, Jordano P, Marquis RJ, Rico-Grey V, Thompson JN (2010) Changes of a mutualistic network over time: reanalysis over a 10-year period. Ecology 9:793–801. doi:10.1890/08-1883.1

    Article  Google Scholar 

  • Dormann CF, Gruber B, Fründ J (2008) Introducing the bipartite package: analysing ecological networks. R News 8:8–11

    Google Scholar 

  • Dormann CF, Fründ J, Bluthgen N, Gruber B (2009) Indices, graphs and null models: analyzing bipartite ecological networks. Open Ecol J 2:7–24

    Article  Google Scholar 

  • Freitas AVL, Oliveira PS (1992) Biology and behavior of Eunica bechina (Lepidoptera: Nymphalidae) with special reference to larval defense against ant predation. J Res Lepidoptera 31:1–11

    Google Scholar 

  • Freitas AVL, Oliveira PS (1996) Ants as selective agents on herbivore biology: effects on the behaviour of a non-myrmecophilous butterfly. J Anim Ecol 65:205–210

    Article  Google Scholar 

  • González-Teuber M, Heil M (2009) The role of extrafloral nectar amino acids for the preferences of facultative and obligate ant mutualists. J Chem Ecol 35:459–468. doi:10.1007/s10886-009-9618-4

    Article  PubMed  Google Scholar 

  • Guimarães PR, Rico-Gray V, Oliveira PS, Izzo TJ, dos Reis SF, Thompson JN (2007) Interaction intimacy affects structure and coevolutionary dynamics in mutualistic networks. Curr Biol 17:1797–1803. doi:10.1016/j.cub.2007.09.059

    Article  PubMed  Google Scholar 

  • Hammer Ø, Harper DAT, Ryan PD (2001) PAST: paleontological statistics software package for education and data analysis. Palaeontologia Electronica 1:9

    Google Scholar 

  • Heil M, McKey D (2003) Protective ant–plant interactions as model systems in ecological and evolutionary research. Annu Rev Ecol Evol Syst 34:425–453

    Article  Google Scholar 

  • Heil M, Fiala B, Maschwitz U, Linsenmair KE (2001) On benefits of indirect defence: short- and long-term studies of antiherbivore protection via mutualistic ants. Oecologia 126:395–403

    Article  Google Scholar 

  • Janzen DH (1966) Coevolution of mutualism between ants and acacias in Central America. Evolution 20:249–275

    Article  Google Scholar 

  • Koptur S (2005) Nectar as Fuel for plant protectors. In: Wackers FL, Van Rijn CJ, Bruin J (eds) Plant-provided food for carnivorous insects: a protective mutualism and its applications. Cambridge University Press, Cambridge, UK, pp 75–108

    Chapter  Google Scholar 

  • Koptur S, William P, Olive Z (2010) Ants and plants with extrafloral nectaries in fire successional habitats on Andros (Bahamas). Florida Entomol 93:89–99. doi:10.1653/024.093.0112

    Article  Google Scholar 

  • Krebs CJ (1989) Ecological methodology. Harper & Row, New York

    Google Scholar 

  • Lange D, Dáttilo W, Del-Claro K (2013) Influence of extrafloral nectary phenology on ant–plant mutualistic networks in a neotropical savanna. Ecol Entomol 38:463–469. doi:10.1111/een.12036

    Article  Google Scholar 

  • Leston D (1973) The ant mosaic—tropical tree crops and the limiting of pests and diseases. Trop Pest Manag 19:311–341. doi:10.1080/09670877309412778

    Article  Google Scholar 

  • Lopes BC (1995) Treehoppers (Homoptera, Membracidae) in southeastern Brazil: use of host plants. Revista Brasileira de Zoologia 12:595–608

    Article  Google Scholar 

  • Machado SR, Morellato LPC, Sajo MJ, Oliveira PS (2008) Morphological patterns of extrafloral nectaries in woody plant species of the Brazilian cerrado. Plant Biol 10:660–673. doi:10.1111/j.1438-8677.2008.00068.x

    Article  CAS  PubMed  Google Scholar 

  • Magurran AE (2004) Measuring biological diversity. Oxford: Blackwell Pub. Malden, MA

  • Majer JD (1990) The abundance and diversity of arboreal ants in Northern Australia. Biotropica 22:191–199

    Article  Google Scholar 

  • Mody K, Linsenmair KE (2004) Plant-attracted ants affect arthropod community structure but not necessarily herbivory. Ecol Entomol 29:217–225

    Article  Google Scholar 

  • Oliveira PS, Brandão CRF (1991) The ant community associated with extrafloral nectaries in the Brazilian cerrados. In: Huxley CR, Cutler DF (eds) Ant–plant interactions. Oxford University Press, Oxford, England, pp 198–212

    Google Scholar 

  • Oliveira PS, Del-Claro K (2005) Multitrophic interactions in a neotropical savanna: ant-hemipteran systems, associated insect herbivores and a host plant. In: Burslem DFRP, Pinard MA, Hartley SA (eds) Biotic interactions in the tropics. Cambridge University Press, Cambridge, pp 414–438

    Chapter  Google Scholar 

  • Oliveira PS, Freitas AVL (2004) Ant-plant-herbivore interactions in the neotropical cerrado savanna. Naturwissenschaften 91:557–570. doi:10.1007/s00114-004-0585-x

    Article  CAS  PubMed  Google Scholar 

  • Oliveira PS, Leitão-Filho HF (1987) Extrafloral nectaries—their taxonomic distribution and abundance in the woody flora of cerrado vegetation in southeast Brazil. Biotropica 19:140–148

    Article  Google Scholar 

  • Oliveira-Filho AT, Rater JA (2002) Vegetation physiognomies and woody flora of the Cerrado biome. In: Oliveira PS, Marquis RJ (eds) The Cerrados of Brazil: ecology and natural history of a neotropical savanna. Columbia University Press, New York, pp 91–120

    Google Scholar 

  • Powell S, Costa AN, Lopes CT, Vasconcelos HL (2011) Canopy connectivity and the availability of diverse nesting resources affect species coexistence in arboreal ants. J Anim Ecol 80:352–360. doi:10.1111/j.1365-2656.2010.01779.x

    Article  PubMed  Google Scholar 

  • R Development Core Team 2012 (2012) R: a language and environment for statistical computing. In: Team RDC (ed) R 2.15.2. R Foundation for Statistical Computing, Vienna, Austria

  • Ribas CR, Schoereder JH (2004) Determining factors of arboreal ant mosaics in Cerrado vegetation (Hymenoptera: formicidae). Sociobiology 44:49–68

    Google Scholar 

  • Ribas CR, Schoereder JH, Pic M, Soares SM (2003) Tree heterogeneity, resource availability, and larger scale processes regulating arboreal ant species richness. Austral Ecol 28:305–314. doi:10.1046/j.1442-9993.2003.01290.x

    Article  Google Scholar 

  • Rico-Gray V, Oliveira PS (2007) The ecology and evolution of ant-plant interactions. University of Chicago Press, Chicago

    Book  Google Scholar 

  • Schoereder JH, Sobrinho TG, Madureira MS, Ribas CR, Oliveira PS (2010) The arboreal ant community visiting extrafloral nectaries in the Neotropical cerrado savanna. Terr Arthropod Rev 3:3–27. doi:10.1163/187498310x487785

    Article  Google Scholar 

  • Sendoya SF, Oliveira PS (2015) Ant-caterpillar antagonism at the community level: interhabitat variation of tritrophic interactions in a neotropical savanna. J Anim Ecol 84:442–452. doi:10.1111/1365-2656.12286

    Article  PubMed  Google Scholar 

  • Sendoya SF, Freitas AVL, Oliveira PS (2009) Egg-laying butterflies distinguish predaceous ants by sight. Am Nat 174:134–140. doi:10.1086/599302

    Article  PubMed  Google Scholar 

  • Staab M, Blüthgen N, Klein AM (2014) Tree diversity alters the structure of a tri-trophic network in a biodiversity experiment. Oikos. doi:10.1111/oik.01723

    Google Scholar 

  • Stadler B, Dixon AFG (2005) Ecology and evolution of aphid-ant interactions. Annu Rev Ecol Evol Syst 36:345–372

    Article  Google Scholar 

  • Styrsky JD, Eubanks MD (2007) Ecological consequences of interactions between ants and honeydew-producing insects. Proc R Soc B Biol Sci 274:151–164

    Article  Google Scholar 

  • Tobin JE, Huxley CR, Cutler DF (1991) A neotropical rainforest canopy, ant community: some ecological considerations. In: Cutler DF, Huxley CR (eds) Ant–plant interactions. Oxford University Press, Oxford, pp 536–538

    Google Scholar 

  • Vazquez DP, Bluthgen N, Cagnolo L, Chacoff NP (2009) Uniting pattern and process in plant–animal mutualistic networks: a review. Ann Bot 103:1445–1457. doi:10.1093/Aob/Mcp057

    Article  PubMed  PubMed Central  Google Scholar 

  • Vazquez DP, Ramos-Jiliberto R, Urbani P, Valdovinos FS (2015) A conceptual framework for studying the strength of plant–animal mutualistic interactions. Ecol Lett 18:385–400. doi:10.1111/ele.12411

    Article  PubMed  Google Scholar 

  • Zuur AF, Ieno EN, Walker N, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. Springer, Dordrecht

    Book  Google Scholar 

Download references

Acknowledgments

We thank B. Dalsgaard, L. Jorge, M. Pareja, P. I. Prado, and S. Ribeiro for comments on the manuscript. G. Bieber, M. Vidal, A. Moreira, H. Soares, L. Sendoya, M. Pareja, and L. Kaminski helped in the field. A. V. Freitas provided valuable logistic support. We thank the Instituto Florestal do Estado de São Paulo, the Clube Caça e Pesca Itororó, and K. Del-Claro for support during fieldwork in Uberlândia. S.F.S. was sponsored by fellowships from the Fundacão de Amparo à Pesquisa do Estado de São Paulo (FAPESP, 07/59881-5, 12/23399-3). P.S.O. was supported by grants from FAPESP (11/18580-8, 12/23671-5, 14/23141-1), the Brazilian Research Council (CNPq, 306115/2013-1), and the Universidade Estadual de Campinas through Faepex.

Author information

Authors and Affiliations

  1. Departamento de Biologia Animal, Universidade Estadual de Campinas, C.P. 6109, Campinas, SP, 13083-970, Brazil

    Sebastian F. Sendoya & Paulo S. Oliveira

  2. Fachbereich Biologie, Technische Universität Darmstadt, Schnittspahnstraße 10, 64287, Darmstadt, Germany

    Nico Blüthgen

  3. Departamento de Biologia Vegetal, Universidade Estadual de Campinas, C.P. 6109, Campinas, SP, 13083-970, Brazil

    Jorge Y. Tamashiro

  4. Facultad de Ciencias, Instituto de Ciencias Naturales, Universidad Nacional de Colombia, AA. 7495, Bogotá DC, Colombia

    Fernando Fernandez

Authors
  1. Sebastian F. Sendoya
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Nico Blüthgen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jorge Y. Tamashiro
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Fernando Fernandez
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Paulo S. Oliveira
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Sebastian F. Sendoya.

Additional information

Handling Editor: Stanislav Gorb.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 73 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sendoya, S.F., Blüthgen, N., Tamashiro, J.Y. et al. Foliage-dwelling ants in a neotropical savanna: effects of plant and insect exudates on ant communities. Arthropod-Plant Interactions 10, 183–195 (2016). https://doi.org/10.1007/s11829-016-9423-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11829-016-9423-2

Keywords

Search

Navigation