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

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Abstract

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.

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References

  • Báez S, Collins SL, Lightfoot D, Koontz TL (2006) Bottom-up regulation of plant community structure in an aridland ecosystem. Ecology 87:2746–2754

    Article  PubMed  Google Scholar 

  • Blüthgen N, Fiedler K (2004) Competition for composition: lessons from nectar-feeding ant communities. Ecology 85:1479–1485

    Article  Google Scholar 

  • Bronstein JL (1998) The contribution of ant-plant protection studies to our understanding of mutualism. Biotropica 30:150–161

    Article  Google Scholar 

  • Bronstein JL, Ruben A, Geber M (2006) The evolution of plant-insect mutualisms. New Phytol 172:412–428

    Article  PubMed  Google Scholar 

  • 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 27:47–65

    Article  Google Scholar 

  • Dáttilo W, Marquitti FMD, Guimarães PR Jr, Izzo TJ (2014) The structure of ant-plant ecological networks: Is abundance enough? Ecology 95:475–485

    Article  PubMed  Google Scholar 

  • 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 91:793–801

    Article  PubMed  Google Scholar 

  • 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 205:754–756

    Article  Google Scholar 

  • 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 275–293

    Google Scholar 

  • Ernest SM, Brown JH (2001) Homeostasis and compensation: the role of species and resources in ecosystem stability. Ecology 82:2118–2132

    Article  Google Scholar 

  • F.A.O. UN (2010) The food and agriculture organization of the United Nations’s. Global forest resources Assessment 2010. FAO Forestry paper, 163

  • Feener DH (1981) Competition between ant species: outcome controlled by parasitic flies. Science 214:815–817

    Article  PubMed  Google Scholar 

  • Feener DH (2000) Is the assembly of ant communities mediated by parasitoids? Oikos 90:79–88

    Article  Google Scholar 

  • 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 4:165–182

    Article  Google Scholar 

  • 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 97:186–192

    Article  Google Scholar 

  • General DM, Alpert GD (2012) A synoptic review of the ant genera (Hymenoptera, Formicidae) of the Philippines. ZooKeys 200:1–111

    Article  PubMed  Google Scholar 

  • Godfray HCJ (2007) Parasitoids. Encyclopedia of Biodiversity. Elsevier, Oxford. online version doi:10.1016/B0-12-226865-2/00218-2 ed. Simon A. Levin

  • Heil M (2004) Direct defense or ecological costs: responses of herbivorous beetles to volatiles released by wild lima bean (Phaseolus lunatus). J Chem Ecol 30:1289–1295

    Article  CAS  PubMed  Google Scholar 

  • Heil M (2008) Indirect defence via tritrophic interactions. New Phytol 178:41–61

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Heraty JM (1985) A revision of the Nearctic Eucharitinae (Hymenoptera: Chalcidoidea: Eucharitidae). Proc Entomol Soc Ontario 116:61–103

    Google Scholar 

  • 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 104–120

    Google Scholar 

  • Heraty JM (2000) Phylogenetic relationships of Oraseminae (Hymenoptera: Eucharitidae). Annu Entomol Soc Am 93:374–390

    Article  Google Scholar 

  • Heraty JM (2002) A revision of the genera of Eucharitidae (Hymenoptera: Chalcidoidea) of the world. Mem Am Entomol Inst 68:1–367

    Google Scholar 

  • Heraty JM, Darling D (1984) Comparative morphology of the planidial larvae of Eucharitidae and Perilampidae (Hymenoptera: Chalcidoidea). Syst Entomol 9:30–328

    Article  Google Scholar 

  • 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 29:544–559

    Article  Google Scholar 

  • Horvitz CC, Schemske DW (1984) Effects of ants and an ant-tended herbivore on seed production of a Neotropical herb. Ecology 65:1369–1378

    Article  Google Scholar 

  • 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 173:521–532

    Article  PubMed  Google Scholar 

  • Karban R, Agrawal AA (2002) Herbivore offense. Annu Rev Ecol Syst 33:641–664

    Article  Google Scholar 

  • Kessler A, Heil M (2011) The multiple faces of indirect defences and their agents of natural selection. Funct Ecol 25:348–357

    Article  Google Scholar 

  • Koptur S (1992) Extrafloral nectary-mediated interactions between insects and plants. Insect Plant Interact 4:81–129

    Google Scholar 

  • 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

  • LeBrun EG (2005) Who’s the top dog in ant communities? Resources, parasitoids, and multiple competitive hierarchies. Oecologia 142:643–652

    Article  PubMed  Google Scholar 

  • Leibold MA (1989) Resource edibility and the effects of predators and productivity on the outcome of trophic interactions. Am Nat 134:922–949

    Article  Google Scholar 

  • McKey D (1974) Adaptive patterns in alkaloid physiology. Am Nat 108:305–320

    Article  Google Scholar 

  • 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):59–65

    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 

  • Molina JE, Wen J, Struwe L (2013) Systematics and biogeography of the non-viny grape relative Leea (Vitaceae). Bot J Linn Soc 171:354–376

    Article  Google Scholar 

  • 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 93:841–849

    Article  Google Scholar 

  • Ness JH, Morris WF, Bronstein JL (2006) Integrating quality and quantity of mutualistic service to contrast ant species protecting Ferocactus wislizeni. Ecology 87(4):912–921

    Article  CAS  PubMed  Google Scholar 

  • O´Dowd DJ, Catchpole EA (1983) Ants and extrafloral nectaries: no evidence for plant protection in Helichrysum spp.—ant interactions. Oecologia 59:191–200

    Article  Google Scholar 

  • Oksanen L, Oksanen T (2000) The logic and realism of the hypothesis of exploitation ecosystems. Am Nat 155:703–723

    Article  PubMed  Google Scholar 

  • 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 99:567–576

    Article  Google Scholar 

  • 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):84

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Power ME (1992) Top-down and bottom-up forces in food webs: do plants have primacy. Ecology 73(3):733–774

    Article  Google Scholar 

  • 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 6:289–295

    Article  Google Scholar 

  • Ridsdale CE (1976) A revision of the tribe Cephalantheae (Rubiaceae). Blumea 23:177–188

    Google Scholar 

  • 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 160:537–549

    Article  PubMed  Google Scholar 

  • Rudgers JA (2004) Enemies of herbivores can shape plant traits: selection in a facultative ant-plant mutualism. Ecology 85(1):192–205

    Article  Google Scholar 

  • Schemske DW (1982) Ecological correlates of a neotropical mutualism: ant assemblages at Costus extrafloral nectaries. Ecology 63:932–941

    Article  Google Scholar 

  • Schmitz OJ (1993) Trophic exploitation in grassland food chains: simple models and a field experiment. Oecologia 93:327–335

    Article  Google Scholar 

  • Thompson JN (1999) Specific hypotheses on the geographic mosaic of coevolution. Am Nat 153:1–14

    Article  Google Scholar 

  • Thompson JN (2006) Mutualistic webs of species. Ecology 312:372–373

    CAS  Google Scholar 

  • Varone L, Briano J (2009) Bionomics of Orasema simplex (Hymenoptera: Eucharitidae), a parasitoid of Solenopsis fire ants (Hymenoptera: Formicidae) in Argentina. Biol Control 48:204–209

    Article  Google Scholar 

  • Vasconcelos HL (1991) Mutualism between Maieta guianensis Abl., a myrmecophytic melastome, and one of its ant inhabitants: ant protection against insect herbivores. Oecologia 87:295–298

    Article  Google Scholar 

  • 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

    Article  PubMed Central  PubMed  Google Scholar 

  • Wilson EO, Durlach NI, Roth LM (1958) Chemical releasers of necrophoric behavior in ants. Psyche 65:108–114

    Article  Google Scholar 

  • Wootton JT (1994) Predicting direct and indirect effects: an integrated approach using experiments and path analysis. Ecology 75:151–165

    Article  Google Scholar 

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Acknowledgments

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.

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Correspondence to Christoph Schwitzke.

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Schwitzke, C., Fiala, B., Linsenmair, K.E. et al. Eucharitid ant-parasitoid affects facultative ant-plant Leea manillensis: top-down effects through three trophic levels. Arthropod-Plant Interactions 9, 497–505 (2015). https://doi.org/10.1007/s11829-015-9391-y

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