Skip to main content
SpringerLink
Log in

Pyrrolizidine alkaloid deters ant predators of Utetheisa ornatrix eggs: effects of alkaloid concentration, oxidation state, and prior exposure of ants to alkaloid-laden prey

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

Abstract

To examine the chemical defense of lepidopteran eggs towards ant predators, eggs of the arctiid moth Utetheisa ornatrix were offered to laboratory colonies of the ant Leptothorax longispinosus. The ants rapidly devoured Utetheisa eggs produced by parents reared on an alkaloid-free diet, but left eggs that had been endowed with parental alkaloid largely unmolested. That defense can be attributed directly to the presence of a pyrrolizidine alkaloid since topical application of monocrotaline in either its free base or N-oxide state conferred protection on otherwise palatable eggs. The N-oxide and free base were not equally effective in conferring protection however; free-base treated eggs were subject to greater predation than N-oxide treated eggs after 24 h. The emergence of differential alkaloid effectiveness only after prolonged exposure is consistent with the notion that chemical protection is seldom absolute. That difference was resolved only when the otherwise food-deprived ants exceeded a certain threshold of hunger. The efficacy of applied monocrotaline as a predator deterrent increased with increasing concentration of N-oxide, but was lowest for eggs treated with an intermediate concentration of free base. The latter concentration effect likely represents an artefact of the behaviour of the ant colonies offered eggs treated with an intermediate concentration, as those colonies were the most voracious predators in reference tests with palatable eggs. In addition to the immediate deterrent value of pyrrolizidine alkaloid, ant colonies that had been exposed to alkaloid-laden eggs subsequently avoided even palatable, unprotected eggs offered 33 days later. Our data provide the first demonstration of such long-term avoidance of chemically protected lepidopteran prey by an invertebrate. The discovery of a mechanism promoting learned avoidance on the part of ant predators has important ramifications to egg-laying strategies of female Utetheisa, both in terms of the dispersion of eggs, and the extent to which eggs are provisioned with alkaloid.

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

  • Alloway TM (1979) Raiding behaviour of two species of slavemaking ants, Harpagoxenus americanus (Emery) and Leptothorax duloticus Wesson (Hymenoptera: Formicidae). Anim Behav 27:202–210

    Google Scholar 

  • Alloway TM, Buschinger A, Talbot M, Stuart R, Thomas C (1982) Polygyny and polydomy in three North American species of the ant genus Leptothorax Mayr (Hymenoptera: Formicidae). Psyche 89:249–274

    Google Scholar 

  • Alloway TM, Leighl A, Ryckman D (1991) Diet does not affect intercolonial fighting in Leptothoracine ants. Ins Soc 38:189–192

    Google Scholar 

  • Ayre GL, Hitchon DE (1968) The predation of tent caterpillars, Malacosoma americanum (Lepidoptera: Lasiocampidae) by ants (Hymenoptera: Formicidae). Can Ent 100:823–826

    Google Scholar 

  • Berenbaum MR, Miliczky E (1984) Mantids and milkweed bugs: efficacy of aposematic coloration against invertebrate predators. Am Midl Nat 111:64–68

    Google Scholar 

  • Bernays EA, Cornelius ML (1989) Generalist caterpillar prey are more palatable than specialists for the generalist predator Iridomyrmex humilis. Oecologia 79:427–430

    Google Scholar 

  • Bhatkar A, Whitcomb WH (1970) Artificial diet for rearing various species of ants. Fla Ent 53:217–232

    Google Scholar 

  • Blaustein AR (1988) Ecological correlates and potential functions of kin recognition and kin association in anuran larvae. Behav Genet 18:449–464

    Google Scholar 

  • Bogner F, Eisner T (1991) Chemical basis of egg cannibalism in a caterpillar (Utetheisa ornatrix). J Chem Ecol 17:2063–2075

    Google Scholar 

  • Boppré M (1990) Lepidoptera and pyrrolizidine alkaloids — exemplification of complexity in chemical ecology. J Chem Ecol 16:165–185

    Google Scholar 

  • Bowers MD, Larin Z (1989) Acquired chemical defense in the lycaenid butterfly, Eumaeus atala. J Chem Ecol 15:1133–1146

    Google Scholar 

  • Buschinger A, Pfeifer E (1988) Effects of nutrition on brood production and slavery in ants (Hymenoptera, Formicidae). Ins Soc 35:61–69

    Google Scholar 

  • Campbell RW, Torgersen TR, Srivastava N (1983) A suggested role for predaceous birds and ants in the population dynamics of the western spruce budworm. For Sci 29:779–790

    Google Scholar 

  • Carson R (1987) Silent Spring (25th anniversary edition). Houghton Mifflin, Boston

    Google Scholar 

  • Conner WE, Eisner T, Vander Meer RK, Guerrero A, Ghiringelli D, Meinwald J (1980) Sex attractant of an arctiid moth (Utetheisa ornatrix): a pulsed chemical signal. Behav Ecol Sociobiol 7:55–63

    Google Scholar 

  • Conner WE, Eisner T, Vander Meer RK, Guerrero A, Meinwald J (1981) Precopulatory sexual interaction in an arctiid moth (Utetheisa ornatrix): role of a pheromone derived from dietary alkaloids. Behav Ecol Sociobiol 9:227–235

    Google Scholar 

  • Conner WE, Roach B, Benedict E, Meinwald J, Eisner T (1990) Courtship pheromone production and body size as correlates of larval diet in males of the arctiid moth, Utetheisa ornatrix. J. Chem Ecol 16:543–552

    Google Scholar 

  • Dussourd DE, Ubik K, Harvis C, Resch J, Meinwald J, Eisner T (1988) Biparental defensive endowment of eggs with acquired plant alkaloid in the moth Utetheisa ornatrix. Proc Natl Acad Sci USA 85:5992–5996

    Google Scholar 

  • Dussourd DE, Harvis CA, Meinwald J, Eisner T (1991) Pheromonal advertisement of a nuptial gift by a male moth (Utetheisa ornatrix). Proc Natl Acad Sci USA 88:9224–9227

    Google Scholar 

  • Eisner T (1982) For the love of nature: exploration and discovery at biological field stations. BioScience 32:321–326

    Google Scholar 

  • Eisner T, Eisner M (1991) Unpalatability of the pyrrolizidine alkaloid-containing moth Utetheisa ornatrix, and its larva, to wolf spiders. Psyche 98:111–118

    Google Scholar 

  • Eisner T, Meinwald YC (1965) Defensive secretion of a caterpillar (Papilio). Science 150:1733–1735

    Google Scholar 

  • Eisner T, Meinwald J (1987) Alkaloid-derived pheromones and sexual selection in Lepidopterea. In: (Prestwich G.D., Blomquist G.J.) (eds) Pheromone Biochemistry Academic Press, Florida, pp 251–269

    Google Scholar 

  • Fiala B, Maschwitz U (1990) Studies of the south east asian antplant association Crematogaster borneensis/Macaranga: adaptations of the ant partner. Ins Soc 37:212–231

    Google Scholar 

  • Hinton HE (1981) Biology of Insect Eggs, Vol. I. Pergamon Press, Oxford

    Google Scholar 

  • Honda K (1983) Defensive potential of components of the larval osmaterial secretion of papilionid butterflies against ants. Physiol Entomol 8:173–179

    Google Scholar 

  • Hrdy I, Jasic J, Novák K, Ruzicka Z, Vallo V, Weismann L, Zeleny J (1968) The sugar-cane borer, Diatraea saccharalis, in Cuba. I. Bionomics and Ecology. Acta ent. bohemoslov. 65:436–457

    Google Scholar 

  • Johnson AE, Molyneux RJ, Merrill GB (1985) Chemistry of toxic range plants. Variation in pyrrolizidine alkaloid content of Senecio, Amsinckia, and Crotalaria species. J Agric Food Chem 33:50–55

    Google Scholar 

  • Kfir A (1992) Seasonal abundance of the stem borer Chilo partellus (Lepidoptera: Pyralidae) and its parasites on summer grain crops. J Econ Entomol 85:518–529

    Google Scholar 

  • Lashomb JH, Metterhouse W, Chianese R (1988) Use of biological control measures in the intensive management of insect pests in New Jersey. Am J Altern Agric 3:77–82

    Google Scholar 

  • Madhun YA, Freed VH (1990) Pesticides in the soil environment: processes, impacts, and modelling. In: H.H.Cheng (ed) Impact of pesticides on the environment Soil Science Society of America, Madison, pp 429–466

    Google Scholar 

  • Martyn EJ (1965) Studies on the ecology of Oncopera intricata Walker (Lepidoptera: Hepialidae). Aust J Zool 13:811–815

    Google Scholar 

  • Mattocks AR (1969) Dihydropyrrolizidine derivatives from unsaturated pyrrolizidine alkaloids. J Chem Soc C Organic 8:1155–1162

    Google Scholar 

  • Mattocks AR (1986) Chemistry and Toxicology of Pyrrolizidine Alkaloids. Academic Press, London

    Google Scholar 

  • Nagy M (1979) The effect of Lepidoptera larvae consumption on the leaf production of Quercus petraea (Matt.) Liebl. Acta Bot Acad Sci Hung 27:141–151

    Google Scholar 

  • Pasteur G (1982) A classificatory review of mimicry systems. Ann Rev Ecol Syst 13:169–199

    Google Scholar 

  • Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225

    Google Scholar 

  • Rothschild M, Alpin RP, Cockrum PA, Edgar JA, Fairweather P, Lees R (1979) Pyrrolizidine alkaloids in arctiid moths (Lep.) with a discussion on host plant relationships and the role of these secondary plant substances in the Arctiidae. Biol J Linn Soc 12:305–326

    Google Scholar 

  • Schneider D (1992) 100 years of pheromone research an essay on Lepidoptera. Naturwissenschaften 79:241–250

    Google Scholar 

  • Sharma RK, Kasture AV, Kapoor KK, Atal CK (1965) Phytochemical investigation of the genus Crotalaria. Part V. Occurrence of tertiary bases and their N-oxides in Indian Crotalaria. Lloydia 28:209–211

    Google Scholar 

  • Sillén-Tullberg B (1988) Evolution of gregariousness in aposematic butterfly larvae: a phylogenetic analysis. Evolution 42:293–305

    Google Scholar 

  • Storey GK, Aneshansley DJ, Eisner T (1991) Parentally provided alkaloid does not protect eggs of Utetheisa ornatrix (Lepidoptera: Arctiidae) against entomopathogenic fungi. J Chem Ecol 17:687–693

    Google Scholar 

  • Tilman D (1978) Cherries, ants and tent caterpillars: timing of nectar production in relation to susceptibility of caterpillars to ant predation. Ecology 59:686–692

    Google Scholar 

  • Vrieling K, Soldaat LL, Smit W (1991) The influence of pyrrolizidine alkaloids of Senecio jacobaea on Tyria jacobaeae, Brachycaudus cardii and Haplothrips senecionis. Neth J. Zool 41:228–239

    Google Scholar 

  • Whitcomb WH (1967) Bollworm predators in Northeast Arkansas. Ark Fm Res 16:2

    Google Scholar 

  • Witz BW (1990) Antipredator mechanisms in arthropods: a twenty year literature survey. Fla Ent 73:71–99

    Google Scholar 

  • Zar JH (1974) Biostatistical Analysis. Prentice-Hall, Englewood Cliffs

    Google Scholar 

Download references

Author information

Author notes

  1. James F. Hare

    Present address: Department of Zoology, Brandon University, R7A 6A9, Brandon, Manitoba, Canada

Authors and Affiliations

  1. Section of Neurobiology and Behavior, Cornell University, Seeley G. Mudd Hall, 14853-2702, Ithaca, NY, USA

    James F. Hare & Thomas Eisner

Authors
  1. James F. Hare
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Thomas Eisner
    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

Hare, J.F., Eisner, T. Pyrrolizidine alkaloid deters ant predators of Utetheisa ornatrix eggs: effects of alkaloid concentration, oxidation state, and prior exposure of ants to alkaloid-laden prey. Oecologia 96, 9–18 (1993). https://doi.org/10.1007/BF00318024

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00318024

Key words

Search

Navigation