Skip to main content
SpringerLink
Log in

Are ant-aphid associations a tritrophic interaction? Oleander aphids and Argentine ants

  • Original Papers
  • Published:
Oecologia Aims and scope Submit manuscript

Summary

Oleander aphids, (Aphis nerii), which are sporadically tended by ants, were used as a moded system to examine whether host plant factors associated with feeding site influenced the formation of ant-aphid associations. Seasonal patterns of host plant utilization and association with attendant ants were examined through bi-weekly censuses of the aphid population feeding on thirty ornamental oleander plands (Nerium oleander) in northern California in 1985 and 1986. Colonies occurred on both developing and senescing plant terminals, including leaf tips, floral structures, and pods. Aphids preferentially colonized leaf terminals early in the season, but showed no preference for feeding site during later periods. Argentine ants (Iridomyrmex humilis) occasionally tended aphid colonies. Colonies on floral tips were three to four times more likely to attract ants than colonies on leaf tips, even though the latter frequently contained more aphids. Ants showed a positive recruitment response to colonies on floral tips, with a significant correlation between colony size and number of ants. There was no recruitment response to colonies on leaf tips. These patterns were reproducible over two years despite large fluctuations in both aphid population density and ant activity. In a laboratory bioassay of aphid palatability, the generalist predator,Hippodamia convergens, took significantly more aphids reared on floral tips compared to those reared on leaf tips. The patterns reported here support the hypothesis that tritrophic factors may be important in modifying higher level arthropod mutualisms.

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

Similar content being viewed by others

References

  • Addicott JF (1978) Competition for mutualists: aphids and ants. Can J Zool 56:2093–2096

    Google Scholar 

  • Aplin TEH (1976) Poisonous Garden Plants and Other Plants Harmful to Man in Australia. Western Australian Department of Agriculture, Bulletin 3964. 58 pp

  • Altieri MA, Annamalae S, Katiyar KP, Flath RA (1982) Effects of plant extracts on the rates of parasitization ofAnagasta kuehniella eggs byTrichogramma pretiosum under greenhouse conditions. Entomophaga 27:431–438

    Google Scholar 

  • Barbosa P, Letourneau DK (1988) Novel Aspects of Insect-Plant Interactions. John Wiley and Sons, New York

    Google Scholar 

  • Bishop YM, Fienberg SE, Holland PW (1975) Discrete Multivariate Analysis: Theory and Practice. MIT Press, Cambridge

    Google Scholar 

  • Bodenheimer FS, Swirski E (1957) The Aphidoidea of the Middle East. Weizmann Science Press of Israel, Jerusalem

    Google Scholar 

  • Botha CEJ, Evert RF, Walmsley RD (1975) Observations of the penetration of the phloem in leaves ofNerium oleander (Linn.) by stylets of the aphidAphis nerii (B. de F.). Protoplasma 86:309–319

    Article  Google Scholar 

  • Bristow CM (1984) Differential benefits from ant attendance to two species of Homoptera on New York ironweed. J Anim Ecol 53:715–726

    Google Scholar 

  • Bristow CM (1991) Why are so few aphids ant-tended? In: Cutler DF, Huxley C (eds) Ant/Plant Interactions. Oxford University Press (in press)

  • Brower LP, Seiber JN, Nelson CJ, Lynch SP, Tuskes PM (1982) Plant-determined variation in the cardenolide content, thinlayer chromatography profiles and emetic potency of monarch butterflies,Danaus plexippus, reared on the milkweed,Asclepias eriocarpa, in California. J Chem Ecol 8:579–633

    Article  CAS  Google Scholar 

  • Buckley R (1987) Ant-plant-Homopteran interactions. Adv Ecol Res 16:53–85

    Google Scholar 

  • Cavill GWK, Robertson PL, Davies NW (1979) An Argentine ant aggregation factor. Experientia 35:889–890

    Article  Google Scholar 

  • Cushman JH, Addicott JF (1989) Intra-and interspecific competition for mutualists: ants as a limited and limiting resource for aphids. Oecologia 79:315–321

    Article  Google Scholar 

  • Cushman JH, Whitham TG (1989) Conditional mutualism in a membracid-ant association: temporal, age-specific, and density-dependent effects. Ecology 70:1040–1047

    Google Scholar 

  • Deneubourg JL, Aron S, Goss S, Pasteels JM (1990) The selforganizing exploratory pattern of the Argentine ant. J Insect Behav 3:159–168

    Google Scholar 

  • Dixon AFG (1985) Aphid Ecology. Blackie, Glasgow, London

    Google Scholar 

  • Ewart WH, Metcalf RL (1956) Preliminary studies of sugars and amino acids in the honeydews of five species of coccids feeding on citrus in California. Ann Entomol Soc Am 49:441–447

    CAS  Google Scholar 

  • Flanders SE (1951) The role of the ant in the biological control of Homopterous insects. Can Entomol 83:93–98

    Google Scholar 

  • Fuller TC, McClintock E (1986) Poisonous Plants of California. California Natural History Guides, 53. University of California Press, Berkeley

    Google Scholar 

  • Greene E (1989) A diet-induced developmental polymorphism in a caterpillar. Science 243:643–646

    Google Scholar 

  • Groeters FR (1989) Geographic and clonal variation in the milkweed-oleander aphid,Aphis nerii (Homoptera: Aphididae), for winged morph production, life history, and morphology in relation to host plant permanence. Evol Ecol 3:327–341

    Google Scholar 

  • Hall GD, Langenheim JH (1986) Within-tree spatial variation in the leaf monoterpenes ofSequoia sempervirens. Biochem Syst Ecol 14:625–632

    CAS  Google Scholar 

  • Hall RW, Ehler LE (1980) Population ecology ofAphis nerii on oleander. Environ Entomol 9:338–344

    Google Scholar 

  • Hawkins BA, Browning HW, Smith Jr. JW (1987) Field evaluation ofAllorhogas pyralophagus imported into Texas for biological control of the stalkborer,Eoreuma loftini, in sugar cane. Entomophaga 32:483–491

    Google Scholar 

  • Hinton HE (1951) Myrmecophilous Lycaenidae and other Lepidoptera—a summary. Proc Trans South Lond Entomol Nat Hist Soc (1949–50), pp 111–175

  • Holldobler B, Wilson EO (1990) The Ants. The Belknap Press of Harvard University Press. Cambridge, MA

    Google Scholar 

  • Hua LZ, Lammers F, van Lenteren JC, Huisman PWT, van Vianen A, de Ponti OMB (1987) The parasite-host relationship betweenEncarsia formosa Gahan andTrialeurodes vaporariorum (Westwood): XXV. Influence of leaf structure on the searching activity ofEncarsia formosa. J Appl Entomol 104:297–304

    Google Scholar 

  • Ismail II, Swailem SM (1971) Seasonal occurrence ofAphis nerii Boyer in Giza region (Egypt). Bull Soc Entomol Egypte 55:231–238

    Google Scholar 

  • Janzen DH (1978) Cicada (Diceroprocta apache (Davis)) mortality by feeding onNerium oleander. Pan-Pac Entomol 54:69–70

    Google Scholar 

  • Klingauf FA (1987) Feeding, adaptation, and excretion. In: Minks AK, Harrewijn P (eds) Aphids: their Biology, Natural Enemies, and Control. vol. A. Elsevier, Amsterdam pp 225–253

    Google Scholar 

  • Krombein KV (1951) Wasp visitors of tulip-tree honeydew at Dunn-Loring, Virginia. Ann Ent Soc Am 41:141–143

    Google Scholar 

  • Lawton JH, McNeill S (1979) Between the devil and the deep blue sea: on the problem of being a herbivore. In: Anderson RM, Turner BD, Taylor LR (eds) Populations Dynamics. Blackwell, Oxford. pp 223–244

    Google Scholar 

  • Malcolm SB (1986) Aposematism in a soft-bodied insect: a case for kin selection. Behav Ecol Sociobiol 18:387–393

    Article  Google Scholar 

  • Malcolm SB (1990) Chemical defence in chewing and sucking insect herbivores: plant-derived cardenolides in the monarch butterfly and oleander aphid. Chemoecol 1:12–21

    CAS  Google Scholar 

  • Mattson WJ (1980) Herbivory in relation to plant nitrogen content. Ann Rev Ecol Syst 11:119–161

    Article  Google Scholar 

  • McLain DK, Shure DJ (1985) Host plant toxins and unpalatability ofNeacoryphus bicrucis. Ecol Entomol 10:291–298

    Google Scholar 

  • McNeil JN, Delisle J, Finnegan RJ (1977) Inventory of aphids on seven conifer species in association with the introduced red wood antFormica lugubris (Hymenoptera: Formicidae). Can Entomol 109:1199–1202

    Google Scholar 

  • Molyneux RJ, Campbell BC, Dreyer DL (1990) Honeydew analysis for detecting phloem transport of plant natural products. J. Chem. Ecol. 16:1899–1909

    Article  CAS  Google Scholar 

  • Nixon GEJ (1951) The Association of Ants with Aphids and Coccids. Commonwealth Instit Entomol Lond. 36 pp

  • Nordlund DA, Chalfant RB, Lewis WJ (1985) Response ofTrichogramma pretiosum females to volatile synomones from tomato plants. J Ent Sci 20:372–376

    Google Scholar 

  • Pierce NE, Elgar MA (1985) The influence of ants on host plant selection byJalmenus evagoras, a myrmecophilous lycaenid butterfly. Behav Ecol Sociobiol 16:209–222

    Article  Google Scholar 

  • Price PW, Bouton CE, Gross P, McPheron BA, Thompson JN, Weis AE (1980) Interactions among three trophic levels: influence of plants on interactions between insect herbivores and natural enemies. Ann Rev Ecol Syst 11:41–65

    Article  Google Scholar 

  • Rothschild M, von Euw J, Reichstein T (1970) Cardiac glycosides in the oleander aphidAphis nerii. J Insect Physiol 16:1191–1195

    Article  Google Scholar 

  • Siegel S (1956) Nonparametric Statistics for the Behavioral Sciences. McGraw-Hill Book Company, New York

    Google Scholar 

  • Smiley JT, Horn JM, Rank NE (1985) Ecological effects of salicin at three trophic levels: new problems from old adaptations. Science 229:649–651

    CAS  Google Scholar 

  • Smith HS, Armitage HM (1931) The biological control of mealybugs attacking citrus. Calif Agric Exp Station Bull 509:1–74

    Google Scholar 

  • Sokal RR, Rohlf FJ (1969) Biometry. W.H. Freeman and Company. San Francisco

    Google Scholar 

  • Sudd JH (1983) The distribution of foraging wood-ants (Formica lugubris Zett.) in relation to the distribution of aphids. Insectes Sociaux, Paris 30:298–307

    Google Scholar 

  • Thorpe KW, Barbosa P (1986) Effect of consumption of high and low nicotine tobacco byManduca sexta on survival of the gregarious endoparasitoidCotesia congregata. J Chem Ecolo 12:1329–1337

    Google Scholar 

  • Way WJ (1963) Mutualism between ants and honeydew-producing Homoptera. Ann Rev Entomol 8:307–344

    Article  Google Scholar 

  • Ward PS (1987) Distribution of the introduced Argentine ant (Iridomyrmex humilis) in natural habitats of the lower Sacramento Valley and its effects on the indigenous ant fauna. Hilgardia 55:1–16

    Google Scholar 

  • Yamauchi T, Abe T, Tachibana Y, Atal CK, Sharma BM, Imre Z (1983) Quantitative variations in the cardiac glycosides of oleander. Phytochemistry 22:2211–2214

    Article  CAS  Google Scholar 

  • Zoebelein G (1956a) Der Honigtau als Nahrung der Insekten. Teil I. Z. Ang Entomol 38:369–416

    Google Scholar 

  • Zoebelein G (1956b) Der Honigtau als Nahrung der Insekten. Teil II. Z Ang Entomol 39:129–167

    CAS  Google Scholar 

  • Zoebelein G (1957) Die Rolle des Waldhonigtaus im Nahrungshaushalt forstlich nutzlicher Insekten. Forstwissenschafliches Zentralblatt 76:24–34

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department or Entomology, Michigan State University, 48824, East Lansing, MI, USA

    C. M. Bristow

Authors
  1. C. M. Bristow
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bristow, C.M. Are ant-aphid associations a tritrophic interaction? Oleander aphids and Argentine ants. Oecologia 87, 514–521 (1991). https://doi.org/10.1007/BF00320414

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00320414

Key words

Search

Navigation