Arthropod-Plant Interactions

, Volume 9, Issue 5, pp 497–505 | Cite as

Eucharitid ant-parasitoid affects facultative ant-plant Leea manillensis: top-down effects through three trophic levels

  • Christoph Schwitzke
  • Brigitte Fiala
  • K. Eduard Linsenmair
  • Eberhard Curio
Original Paper


Facultative ant–plant mutualisms are variable systems, shaped by a number of biotic and abiotic factors. Especially in tropical ecosystems, the generally assumed mutualistic benefits are often hard to prove. We studied the system Leea manillensis on the Philippine island Panay and its indirect defence mechanism against herbivory by producing extrafloral nectar therewith attracting ants. Unexpectedly, we found an ant-parasitoid wasp from the genus Chalcura (Eucharitidae) to have a strong influence on the system, on ants as well as on plants. The parasitoid not only altered the behaviour of interacting ant species, but also directly and indirectly affected the plants’ fitness. This study demonstrates how top-down effects may alter species interactions and have a massive effect on mutualisms and their beneficial outcome.


Chalcura Extrafloral nectaries Ants Mutualistic interaction Philippines 



The study was generously supported by the DAAD (German Academic Exchange Service). We are very grateful to the Philippine NGO PhilinCon and the staff of the research station Sibaliw for their support, especially Benjamin S. Tacud jr. and Junmar E. Jamangal. We thank the PASU Rhodel B. Lababit (DENR) for the generous permission to work at the NW Panay Natural Park. We also thank Stefan Schmidt (ZMS) for the determination of the parasitoid wasp.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

11829_2015_9391_MOESM1_ESM.pdf (563 kb)
Supplementary material 1 (PDF 563 kb)
11829_2015_9391_MOESM2_ESM.pdf (401 kb)
Supplementary material 2 (PDF 401 kb)
11829_2015_9391_MOESM3_ESM.pdf (383 kb)
Supplementary material 3 (PDF 382 kb)
11829_2015_9391_MOESM4_ESM.pdf (436 kb)
Supplementary material 4 (PDF 436 kb)


  1. Báez S, Collins SL, Lightfoot D, Koontz TL (2006) Bottom-up regulation of plant community structure in an aridland ecosystem. Ecology 87:2746–2754CrossRefPubMedGoogle Scholar
  2. Blüthgen N, Fiedler K (2004) Competition for composition: lessons from nectar-feeding ant communities. Ecology 85:1479–1485CrossRefGoogle Scholar
  3. Bronstein JL (1998) The contribution of ant-plant protection studies to our understanding of mutualism. Biotropica 30:150–161CrossRefGoogle Scholar
  4. Bronstein JL, Ruben A, Geber M (2006) The evolution of plant-insect mutualisms. New Phytol 172:412–428CrossRefPubMedGoogle Scholar
  5. Carey B, Visscher K, Heraty JM (2012) Nectary use for gaining access to an ant host by the parasitoid Orasema simulatrix (Hymenoptera, Eucharitidae). J Hymenop Res 27:47–65CrossRefGoogle Scholar
  6. Dáttilo W, Marquitti FMD, Guimarães PR Jr, Izzo TJ (2014) The structure of ant-plant ecological networks: Is abundance enough? Ecology 95:475–485CrossRefPubMedGoogle Scholar
  7. Dìaz-Castelazo C, Guimarães PR Jr, Jordano P, Thompson JN, Marquis RJ (2010) Changes of a mutualistic network over time: reanalysis over a 10-year period. Ecology 91:793–801CrossRefPubMedGoogle Scholar
  8. do Nascimento EA, Del-Claro K (2010) Ant visitation to extrafloral nectaries decreases herbivory and increases fruit set in Chamaecrista debilis (Fabaceae) in a Neotropical savanna. Flora 205:754–756CrossRefGoogle Scholar
  9. Dyer LA (2008) The ecology of tri-trophic interactions in the tropics. In: Carson WP, Schnitzer SA (eds) Tropical forest community ecology. Blackwell Science, Oxford, pp 275–293Google Scholar
  10. Ernest SM, Brown JH (2001) Homeostasis and compensation: the role of species and resources in ecosystem stability. Ecology 82:2118–2132CrossRefGoogle Scholar
  11. F.A.O. UN (2010) The food and agriculture organization of the United Nations’s. Global forest resources Assessment 2010. FAO Forestry paper, 163Google Scholar
  12. Feener DH (1981) Competition between ant species: outcome controlled by parasitic flies. Science 214:815–817CrossRefPubMedGoogle Scholar
  13. Feener DH (2000) Is the assembly of ant communities mediated by parasitoids? Oikos 90:79–88CrossRefGoogle Scholar
  14. Fiala B, Linsenmair KE (1995) Distribution and abundance of plants with extrafloral nectaries in the woody flora of a lowland primary forest in Malaysia. Biodiv Cons 4:165–182CrossRefGoogle Scholar
  15. Fiala B, Grunsky H, Maschwitz U, Linsenmair KE (1994) Diversity of ant-plant interactions: protective efficacy in Macaranga species with different degrees of ant association. Oecologia 97:186–192CrossRefGoogle Scholar
  16. General DM, Alpert GD (2012) A synoptic review of the ant genera (Hymenoptera, Formicidae) of the Philippines. ZooKeys 200:1–111CrossRefPubMedGoogle Scholar
  17. Godfray HCJ (2007) Parasitoids. Encyclopedia of Biodiversity. Elsevier, Oxford. online version doi: 10.1016/B0-12-226865-2/00218-2 ed. Simon A. Levin
  18. Heil M (2004) Direct defense or ecological costs: responses of herbivorous beetles to volatiles released by wild lima bean (Phaseolus lunatus). J Chem Ecol 30:1289–1295CrossRefPubMedGoogle Scholar
  19. Heil M (2008) Indirect defence via tritrophic interactions. New Phytol 178:41–61CrossRefPubMedGoogle Scholar
  20. Heil M, McKey D (2003) Protective ant-plant interactions as model systems in ecological and evolutionary research. Annu Rev Ecol Syst 34:425–453CrossRefGoogle Scholar
  21. Heraty JM (1985) A revision of the Nearctic Eucharitinae (Hymenoptera: Chalcidoidea: Eucharitidae). Proc Entomol Soc Ontario 116:61–103Google Scholar
  22. Heraty JM (1994) Biology and importance of two eucharitid parasites of Wasmannia and Solenopsis. In: Williams DR (ed) Exotic ants. Biology, impact and control of induced species. Westview Press, Boulder, pp 104–120Google Scholar
  23. Heraty JM (2000) Phylogenetic relationships of Oraseminae (Hymenoptera: Eucharitidae). Annu Entomol Soc Am 93:374–390CrossRefGoogle Scholar
  24. Heraty JM (2002) A revision of the genera of Eucharitidae (Hymenoptera: Chalcidoidea) of the world. Mem Am Entomol Inst 68:1–367Google Scholar
  25. Heraty JM, Darling D (1984) Comparative morphology of the planidial larvae of Eucharitidae and Perilampidae (Hymenoptera: Chalcidoidea). Syst Entomol 9:30–328CrossRefGoogle Scholar
  26. Heraty J, Hawks D, Kostecki JS, Carmichael A (2004) Phylogeny and behaviour of the Gollumiellinae, a new subfamily of the ant-parasitic Eucharitidae (Hymenoptera: Chalcidoidea). Syst Ent 29:544–559CrossRefGoogle Scholar
  27. Horvitz CC, Schemske DW (1984) Effects of ants and an ant-tended herbivore on seed production of a Neotropical herb. Ecology 65:1369–1378CrossRefGoogle Scholar
  28. Hrcek J, Miller SE, Whitfield JB, Shima H, Novotny V (2013) Parasitism rate, parasitoid community composition and host specificity on exposed and semi-concealed caterpillars from a tropical rainforest. Oecologia 173:521–532CrossRefPubMedGoogle Scholar
  29. Karban R, Agrawal AA (2002) Herbivore offense. Annu Rev Ecol Syst 33:641–664CrossRefGoogle Scholar
  30. Kessler A, Heil M (2011) The multiple faces of indirect defences and their agents of natural selection. Funct Ecol 25:348–357CrossRefGoogle Scholar
  31. Koptur S (1992) Extrafloral nectary-mediated interactions between insects and plants. Insect Plant Interact 4:81–129Google Scholar
  32. Lachaud J-P, Pèrez-Lachaud G (2012) Diversity of species and behavior of hymenopteran parasitoids of ants: a review. Psyche Article ID 134746. DOI: 10.1155/2012/134746
  33. LeBrun EG (2005) Who’s the top dog in ant communities? Resources, parasitoids, and multiple competitive hierarchies. Oecologia 142:643–652CrossRefPubMedGoogle Scholar
  34. Leibold MA (1989) Resource edibility and the effects of predators and productivity on the outcome of trophic interactions. Am Nat 134:922–949CrossRefGoogle Scholar
  35. McKey D (1974) Adaptive patterns in alkaloid physiology. Am Nat 108:305–320CrossRefGoogle Scholar
  36. Meng L-Z, Martin K, Liu J-X, Chen J (2011) Young leaf protection in the shrub Leea glabra in south-west China: the role of extrafloral nectaries and ants. Arthropod-Plant Interact 6(1):59–65CrossRefGoogle Scholar
  37. Mody K, Linsenmair KE (2004) Plant-attracted ants affect arthropod community structure but not necessarily herbivory. Ecol Entomol 29:217–225CrossRefGoogle Scholar
  38. Molina JE, Wen J, Struwe L (2013) Systematics and biogeography of the non-viny grape relative Leea (Vitaceae). Bot J Linn Soc 171:354–376CrossRefGoogle Scholar
  39. Morrison LW (2000) Mechanisms of Pseudacteon parasitoid (Diptera: Phoridae) effects on exploitative and interference competition in host Solenopsis ants (Hymenoptera: Formicidae). Ann Entomol Soc Am 93:841–849CrossRefGoogle Scholar
  40. Ness JH, Morris WF, Bronstein JL (2006) Integrating quality and quantity of mutualistic service to contrast ant species protecting Ferocactus wislizeni. Ecology 87(4):912–921CrossRefPubMedGoogle Scholar
  41. O´Dowd DJ, Catchpole EA (1983) Ants and extrafloral nectaries: no evidence for plant protection in Helichrysum spp.—ant interactions. Oecologia 59:191–200CrossRefGoogle Scholar
  42. Oksanen L, Oksanen T (2000) The logic and realism of the hypothesis of exploitation ecosystems. Am Nat 155:703–723CrossRefPubMedGoogle Scholar
  43. Pérez-Lachaud G, Heraty JM, Carmichael A, Lachaud J (2006) Biology and behavior of kapala (Hymenoptera: Eucharitidae) attacking Ectatomma, Gnamptogenys, and Pachycondyla (Formicidae and Ponerinae) in Chiapas, Mexico. Ann Entomol Soc Am 99:567–576CrossRefGoogle Scholar
  44. Pires LP, Del-Claro K (2014) Variation in the outcomes of an ant-plant system: fire and leaf fungus infection reduce benefits to plants with extrafloral nectaries. J Insect Sci 14(1):84CrossRefPubMedCentralPubMedGoogle Scholar
  45. Power ME (1992) Top-down and bottom-up forces in food webs: do plants have primacy. Ecology 73(3):733–774CrossRefGoogle Scholar
  46. Rico-Gray V, Díaz-Castelazo C, Ramírez-Hernández A, Guimaraes PR Jr, Holland JN (2012) Abiotic factors shape temporal variation in the structure of an ant-plant network. Arthropod-Plant Interact 6:289–295CrossRefGoogle Scholar
  47. Ridsdale CE (1976) A revision of the tribe Cephalantheae (Rubiaceae). Blumea 23:177–188Google Scholar
  48. Rosumek BF, Fernando FAO, Neves FDeS, Barbosa NPDeU, Diniz L, Oki Y, Pezzini F, Fernandes GW, Cornelissen T (2009) Ants on plants: a meta-analysis of the role of ants as plant biotic defenses. Oecologia 160:537–549CrossRefPubMedGoogle Scholar
  49. Rudgers JA (2004) Enemies of herbivores can shape plant traits: selection in a facultative ant-plant mutualism. Ecology 85(1):192–205CrossRefGoogle Scholar
  50. Schemske DW (1982) Ecological correlates of a neotropical mutualism: ant assemblages at Costus extrafloral nectaries. Ecology 63:932–941CrossRefGoogle Scholar
  51. Schmitz OJ (1993) Trophic exploitation in grassland food chains: simple models and a field experiment. Oecologia 93:327–335CrossRefGoogle Scholar
  52. Thompson JN (1999) Specific hypotheses on the geographic mosaic of coevolution. Am Nat 153:1–14CrossRefGoogle Scholar
  53. Thompson JN (2006) Mutualistic webs of species. Ecology 312:372–373Google Scholar
  54. Varone L, Briano J (2009) Bionomics of Orasema simplex (Hymenoptera: Eucharitidae), a parasitoid of Solenopsis fire ants (Hymenoptera: Formicidae) in Argentina. Biol Control 48:204–209CrossRefGoogle Scholar
  55. Vasconcelos HL (1991) Mutualism between Maieta guianensis Abl., a myrmecophytic melastome, and one of its ant inhabitants: ant protection against insect herbivores. Oecologia 87:295–298CrossRefGoogle Scholar
  56. Veijalainen A, Wahlberg N, Broad GR, Erwin TL, Longino JT, Sääksjärvi IE (2012) Unprecedented ichneumonid parasitoid wasp diversity in tropical forests. Proc Biol Sci 279:4694–4698. doi: 10.1098/rspb.2012.1664 CrossRefPubMedCentralPubMedGoogle Scholar
  57. Wilson EO, Durlach NI, Roth LM (1958) Chemical releasers of necrophoric behavior in ants. Psyche 65:108–114CrossRefGoogle Scholar
  58. Wootton JT (1994) Predicting direct and indirect effects: an integrated approach using experiments and path analysis. Ecology 75:151–165CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2015

Authors and Affiliations

  • Christoph Schwitzke
    • 1
  • Brigitte Fiala
    • 1
  • K. Eduard Linsenmair
    • 1
  • Eberhard Curio
    • 2
  1. 1.Department of Animal Ecology and Tropical BiologyBiozentrumWürzburgGermany
  2. 2.Conservation Biology UnitRuhr-Universität BochumBochumGermany

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