Abstract
Understanding the interactions among plants, hemipterans, and ants has provided numerous insights into a range of ecological and evolutionary processes. In these systems, however, studies concerning the isolated direct and indirect effects of aphid colonies on host plant and other herbivores remain rare at best. The aphid Uroleucon erigeronensis forms dense colonies on the apical shoots of the host plant Baccharis dracunculilfolia (Asteraceae). The honeydew produced by these aphids attracts several species of ants that might interfere with other herbivores. Four hypotheses were tested in this system: (1) ants tending aphids reduce the abundance of other herbivores; (2) the effects of ants and aphids upon herbivores differ between chewing and fluid-sucking herbivores; (3) aphids alone reduce the abundance of other herbivores; and (4), the aphid presence negatively affects B. dracunculifolia shoot growth. The hypotheses were evaluated with ant and aphid exclusion experiments, on isolated plant shoots, along six consecutive months. We adjusted linear mixed-effects models for longitudinal data (repeated measures), with nested spatial random effect. The results showed that: (1) herbivore abundance was lower on shoots with aphids than on shoots without aphids, and even lower on shoots with aphids and ants; (2) both chewing and fluid-sucking insects responded similarly to the treatment, and (3) aphid presence affected negatively B. dracunculifolia shoot growth. Thus, since aphids alone changed plant growth and the abundance of insect herbivores, we suggest that the ant–aphid association is important to the organization of the system B. dracunculifolia-herbivorous insects.
Similar content being viewed by others
References
Abe Y (1988) Trophobiosis between the gall wasp Andricus symbioticus, and the gall-attending ant, Lasius niger. Appl Entomol Zool 23:41–44
Barroso GM (1976) Compositae—subtribo Baccharidinae Hoffman: estudo das espécies ocorrentes no Brasil. Rodriguesia 40:3–273
Bolton B (1994) Identification guide to the ant genera of the world. Harvard University Press, Cambridge
Bonsall MB, Hassell MP (1997) Apparent competition structures ecological assemblages. Nature 388:371–373
Borror DJ, Triplehorn CA, Johnson NF (2002) An introduction to the study of insects. Saunders College Publing, Philadelphia
Bronstein JL (1998) The contribution of ant-plant protection studies to our understanding of mutualism. Biotropica 30:150–161
Buckley YM, Briese DT, Rees M (2003) Demography and management of the invasive plant species Hypericum perforatum I. using multi-level mixed-effects models for characterizing growth, survival and fecundity in a long-term data set. J Applied Ecol 40:481–493
Crawley MJ (2002) Statistical computing: an introduction to data analysis using S-plus. Wiley, Chichester
Dansa CVA, Rocha CFD (1992) An ant-membracid-plant interaction in a cerrado area of Brazil. J Trop Ecol 8:339–348
Delabie JHC (2001) Trophobiosis between Formicidae and Hemiptera (Sternorrhyncha and Auchernorryncha): an overview. Neotrop Entomol 30:501–516
Del-Claro K, Oliveira PS (1999) Ant-Homoptera interactions in a neotropical savana: the honeydew-producing treehopper Guauaquila xiphias (Membracidae) and its associated ant fauna on Didymopanax vinosum (Araliaceae). Biotropica 31:135–144
Del-Claro K, Oliveira PS (2000) Conditional outcomes in a Neotropical treehoper-ant association: temporal and species-specific variation in ant protection and homopteran fecundity. Oecologia 124:156–165
Denno FR, Perfect TJ (1994) Planthoppers: their ecology and management. Chapman & Hall, London
Denno RF, Gratton C, Peterson MA, Langellotto GA, Finke DL, Huberty AF (1995) Bottom-Up forces mediate natural-enemy impact in a phytophagous insect community. Ecology 83:1443–1458
Dyer LA, Lettourneau DK (1999) Relative strengths of top-dow and bottom-up forces in a tropical forest community. Oecologia 119:265–274
Espírito-Santo MM, Fernandes GW (1998) Abundance of Baccharopelma baccharidis (Homoptera: Psyllidae) galls on the dioecious shrub Baccharis dracunculifolia (Asteraceae). Environ Entomol 27:870–876
Espírito-Santo MM, Madeira BG, Neves FS, Faria ML, Fagundes M, Fernandes GW (2003) Sexual differences in reproductive phenology and their consequences for the demography of Baccharis dracunculilfolia (Asteraceae), a dioecious tropical shrub. Ann Bot 91:13–19
Fagundes M, Fernandes GW (2011) Insect herbivores associated with Baccharis dracunculifolia (Asteraceae): responses of gall forming and free-feeding insect herbivores to latitudinal variations. Rev Bio Trop 59:76–89
Fagundes M, Neves FS, Fernandes GW (2005) Direct and indirect interactions involving ants, insect herbivores, parasitoids and the host plant Baccharis dracunculifolia (Asteraceae). Ecol Entomol 30:28–35
Fay PA, Hartnett DC, Knapp AK (1996) Plant tolerance of gall-insect attack and gall-insect performance. Ecology 77:521–534
Fernandes GW, Fagundes M, Woodman RL, Price PW (1999) Ant effects on three-trophic level interactions: plant, galls, and parasitoids. Ecol Entomol 34:411–415
Flatt T, Weisser WW (2000) The effects of mutualistic ants on aphid life history traits. Ecology 38:535–536
Gaume L, McKey D, Anstett MC (1997) Benefits conferred by “timid” ants: active anti-herbivore protection of the rainforest tree Leonardoxa africana by the minute ant Petalomyrmex phylax. Oecologia 112:209–216
Heil M, McKey D (2003) Protective ant-plant interactions as model systems in ecological and evolutionary research. Annu Rev Ecol Evol Syst 34:425–553
Hölldolbler B, Wilson EO (1990) The ants. Cambridge University Press, Mass
Holt RD, Lawton JH (1993) Apparent competition and enemy-free space in insect host-parasitoid communities. Am Nat 142:623–645
Izzo TJ, Julião GR, Almada ED, Fernandes GW (2006) Hiding from defenders: localized chemical modification on the leaves of an Amazonian ant-plant induced by a gall-making insect (Diptera: Cecidomyiidae). Sociobiology 48:417–426
Jolivet P (1996) Ants and plants: an example of coevolution. Backhuys Publishers, Leiden
Larson KC, Whitham TG (1997) Competition between gall aphids and natural plant sinks: plant architecture affects resistance to galling. Oecologia 109:575–582
Majer JD, Delabie JHC, Smith MRB (1994) Arboreal ant community patterns in Cocoa farms, of the arboreal ant mosaic in Ghana, Brazil, Papua New Guinea and Australia–its structure and influence on arthropod diversity. Biotropica 26:73–83
Mody K, Linsenmair KE (2004) Plant-attracted ants affect arthropod community structure but not necessarily herbivory. Ecol Entomol 29:217–225
Moran CV, Southwood TRE (1982) The guild composition of arthropod communities in trees. J Animal Ecol 51:289–306
Morris RJ, Lewis OT, Godfray HCJ (2004) Experimental evidence for apparent competition in a tropical forest food web. Nature 428:310–313
Müller CB, Godfray HCJ (1997) Apparent competition between two aphids species. J Animal Ecol 66:57–64
Oliveira PS, Rico-Gray V, Diaz-Castelazo C, Castillo-Guevara C (1999) Interaction between ants, extraforal nectaries and insect herbivores in Neotropical coastal sand dunes: herbivore deterrence by visiting ants increases fruit set en Opuntia stricta (Cactaceae). Funct Ecol 13:623–631
Price PW, Bouton BE, Gross P, McPheron BA, Thompson JN, Weis AE (1980) Interaction among three trophic levels: influence of plant on interactions between insect herbivores and natural enemies. Annu Rev Ecol Evol Syst 11:41–65
R Development core team (2005) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL http://www.R-project.org
Rosumek FB, Silveira FAO, Neves FS, Barbosa NPU, 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
Sperber CF, Nakayama K, Valverde MJ, Neves FS (2004) Tree species richness and density affect parasitoid diversity in cacao agroforestry. Basic Appl Ecol 5:241–251
Stadler B, Dixon AFG (1999) Ant attendance in aphids: why different degrees of myrmecophily? Ecol Entomol 24:363–369
Stadler B, Dixon AFG (2005) Ecology and evolution of aphid-ant interactions. Annu Rev Ecol Evol Syst 36:345–372
Strong DR, Lawton JH, Southwood TRE (1984) Insects on plants: community patterns and mechanisms. Blackwell Scientific Publication, Cambridge
Styrsky JD, Eubanks MD (2007) Ecological consequences of interactions between ants and honeydew-producing insects. Proc R Soc Lond B 274:151–164
Way MJ (1963) Mutualism between ants and honeydew producing Homoptera. Annu Rev Entomol 8:307–344
Woodman RL, Price PW (1992) Differential larval predation by ants can influence willow sawfly community structure. Ecology 73:1028–1037
Acknowledgments
We thank C.R. Ribas, J.H. Schoereder, B.G. Madeira, A. Janssen (Visiting Teacher on a CAPES grant) and two anonymous reviewers for valuable suggestions on the manuscript. The study was supported by CNPq (472491/2003-2, 309633/2007-9, 476178/2008-8) and Fapemig (CRA 583/01, 697/06, EDT–465/07). M. Fagundes (EDT 25026/05) and F.S. Neves (EDT 25027/05) were supported by FAPEMIG through researcher grant fellowships.
Author information
Authors and Affiliations
Corresponding author
Additional information
Handling Editors: Joseph Dickens and Heikki Hokkanen.
Rights and permissions
About this article
Cite this article
de Siqueira Neves, F., Fagundes, M., Sperber, C.F. et al. Tri-trophic level interactions affect host plant development and abundance of insect herbivores. Arthropod-Plant Interactions 5, 351–357 (2011). https://doi.org/10.1007/s11829-011-9139-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11829-011-9139-2