Skip to main content
Log in

Genetically-based plant resistance traits affect arthropods, fungi, and birds

  • Community Ecology
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

We examine how the distribution of a leafgalling aphid (Pemphigus betae) affects other species associated with natural stands of hybrid cottonwoods (Populus angustifolia x P. fremontii). Aphid transfers on common-garden clones and RFLP analysis show that resistance to aphids in cottonwoods is affected by plant genotype. Because susceptible trees typically support thousands of galls, while adjacent resistant trees have few or none, plant resistance traits that affect the distribution of this abundant herbivore may directly and/or indirectly affect other species. We found that the arthropod community of aphid-susceptible trees had 31% greater species richness and 26% greater relative abundance than aphid-resistant trees. To examine direct and indirect effects of plant resistance traits on other organisms, we experimentally excluded aphids and found that abundances and/or foraging behavior of arthropods, fungi, and birds were altered. First, exclusion of gall aphids on susceptible trees resulted in a 24% decrease in species richness and a 28% decrease in relative abundance of the arthropod community. Second, exclusion of aphids also caused a 2- to 3-fold decrease in foraging and/or presence of three taxa of aphid enemies: birds, fungi, and insects. Lastly, aphidexclussion resulted in a 2-fold increase in inquilines (animals who live in abodes properly belonging to another). We also found that fungi and birds responded to variation in gall density at the branch level. We conclude plant resistance traits affect diverse species from three trophic levels supporting a “bottom-up” influence of plants on community structure.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Atlegrim O (1989) Exclusion of birds from bilberry stands: impact on insect larval density and damage to the bilberry. Oecologia 79: 136–139

    Google Scholar 

  • Boecklen WJ, Price PW (1991) Nonequilibrial community structure of sawflies on arroyo willow. Oecologia 85: 483–491

    Google Scholar 

  • Brown JH, Heske EJ (1990) Control of a desert-grassland transition by a keystone rodent guild. Science 250: 1705–1707

    Google Scholar 

  • Campbell RK, Eikenbary RD (1990) Aphid-plant genotype interactions. Elsevier, Amsterdam

    Google Scholar 

  • Christensen KM, Whitham TG (1991) Indirect herbivore mediation of avian seed dispersal in pinyon pine. Ecology 72: 534–542

    Google Scholar 

  • Christensen KM, Whitham TG (1993) Impact of insect herbivores on competition between birds and mammals for pinyon pine seeds. Ecology 74: 2270–2278

    Google Scholar 

  • Dixon AFG (1985) Aphid ecology. Chapman and Hall, New York

    Google Scholar 

  • Dunson WA, Travis J (1991) The role of abiotic factors in community organization. Am Nat 138: 1067–1091

    Google Scholar 

  • Eckenwalder JE (1984) Natural intersectional hybridization between North American species of Populus (Salicaceae) in sections Aigeiros and Tacamahaca. II. Taxonomy. Can J Bot 62: 325–335

    Google Scholar 

  • Fedde GF (1973) Impact of the balsam wooly aphid (Homoptera: Phylloxeridae) on cones and seed produced by infested Fraser fir. Can Entomol 105: 673–680

    Google Scholar 

  • Feeny P (1976) Plant aparency and chemical defense. In: Wallace JW, Mansell RL (eds) Biochemical interaction between plant and insects. Plenum, New York, pp 1–40

    Google Scholar 

  • Finch DM, Ruggiero LF (1993) Wildlife habitats and biological diversity in the Rocky Mountains and northern Great Plains. Natural Areas J 13: 191–203

    Google Scholar 

  • Floate KD, Whitham TG (1993) The “hybrid bridge” hypothesis: host shifting via plant hybrid swarms. Am Nat 141: 651–662

    Google Scholar 

  • Floate KD, Whitham TG (1995) Insects as traits in plant systematics: their use in discriminating between hybrid cottonwoods. Can J Bot 73: 1–13

    Google Scholar 

  • Fritz RS, Price PW (1988) Genetic variation among plants and insect community structure: willows and sawflies. Ecology 69: 845–856

    Google Scholar 

  • Fritz RS, Simms EL (1992) Plant resistance to herbivores and pathogens. The University of Chicago Press, Chicago

    Google Scholar 

  • Gehring CA, Whitham TG (1991) Herbivore-driven mycorrhizal mutualism in insect-susceptible pinyon pine. Nature 353: 556–557

    Google Scholar 

  • Grier CC, Vogt DJ (1990) Effects of aphid honeydew on soil nitrogen availability and net primary production in an Alnus rubra plantation in western Washington. Oikos 57: 114–118

    Google Scholar 

  • Grigarick AA, Lange WH (1968) Seasonal development and emergence of two species of gall-forming aphids, Pemphigus bursarius and Pemphigus nortoni, associated with poplar trees in California. Ann Entomol Soc Am 61: 509–514

    Google Scholar 

  • Hare JD (1992) Effects of plant variation on herbivore-natural enemy interactions. In: Fritz RS, Simms EL (eds) Plant resistance to herbivores and pathogens. The University of Chicago Press, Chicago, pp 278–298

    Google Scholar 

  • Harper AM (1959) Gall aphids of poplar in Alberta. II. Periods of emergence from galls, reproductive capacities, and predators of aphids in galls. Can Entomol 91: 680–685

    Google Scholar 

  • Kearsley MJC, Whitham TG (1989) Developmental changes in resistance to herbivory: implications for individuals and populations. Ecology 70: 422–434

    Google Scholar 

  • Keim P, Paige KN, Whitham TG, Lark KG (1989) Genetic analysis of an interspecific hybrid swarm of Populus: occurrence of unidirectional introgression. Genetics 123: 557–565

    Google Scholar 

  • Kerbes RH, Kotanen PM, Jefferies RL (1990) Destruction of wetland habitats by lesser snow geese: a keystone species of the west coast of Hudson Bay. J Appl Ecol 27: 242–258

    Google Scholar 

  • Larson KC (1989) Sink-source interaction between a galling aphid and its narrowleaf cottonwood host: within and between plant variation. Ph.D. thesis, Northern Arizona University, Flagstaff, Ariz

  • Larson KC, Whitham TG (1991) Manipulation of food resources by a gall-forming aphid: the physiology of sink-source interactions. Oecologia 88: 15–21

    Google Scholar 

  • Llewellyn M (1972) The effects of the lime aphid, Eucallipterus tiliae L. (Aphididae) on the growth of the lime Tilia x Vulgaris Hayne. I. Energy requirements of the aphid population. J Appl Ecol 9: 261–282

    Google Scholar 

  • Maddox GD, Root RB (1987) Resistance to sixteen diverse species of herbivorous insects within a population of goldenrod, Solidago altissima: genetic variation and heritability. Oecologia 72: 8–14

    Google Scholar 

  • Marquis RJ, Whelan CJ (1994) Insectivorous birds increase growth of white oak through consumption of leaf-chewing insects. Ecology 75: 2007–2014

    Google Scholar 

  • Martinsen GD, Whitham TG (1994) More bird nests in hybrid cottonwood trees. Wilson Bull 106: 474–481

    Google Scholar 

  • Matson PA, Hunter MD (1992) The relative contributions of top-down and bottom-up forces in population and community ecology. Ecology 73: 723–765

    Google Scholar 

  • Mopper S, Mitton JB, Whitham TG, Cobb NS, Christensen KM (1991) Genetic differentiation and heterozygosity associated with resistance to herbivory and environmental stress. Evolution 45: 989–999

    Google Scholar 

  • Moran NA, Whitham TG (1990) Differential colonization of resistant and susceptible host plants: Pemphigus and Populus. Ecology 71: 1059–1067

    Google Scholar 

  • Neill WE, Peacock A (1980) Breaking the bottleneck interactions of invertebrate predators and nutrients in oligotrophic lakes. In: Kerfoot WC (ed) Evolution and ecology of zooplankton communities. University Press of New England, Hanover, pp 715–724

    Google Scholar 

  • Paige KN, Capman WC (1993) The effects of host-plant genotype, hybridization, and environment on gall-aphid attack and survival in cottonwood: the importance of genetic studies and the utility of RFLPs. Evolution 47: 36–45

    Google Scholar 

  • Paige KN, Keim P, Whitham TG, Lark KG (1990) The use of restriction fragment length polymorphisms to study the ecology and evolutionary biology of aphid-plant interaction. In: Campbell RK, Eikenbary RD (eds) Aphid-plant genotype interactions. Elsevier, Amsterdam, pp 69–87

    Google Scholar 

  • Paine RT (1966) Food web complexity and species diversity. Am Nat 100: 65–75

    Google Scholar 

  • Price PW, Bouton CE, Gross P, McPheron BA, Thompson JN, Weis AE (1980) Interaction among three trophic levels: influence of plants on interactions between insect herbivores and natural enemies. Annu Rev Ecol Syst 11: 14–65

    Google Scholar 

  • Rhoades DF, Cates RG (1976) Toward a general theory of plant anti-herbivore chemistry. In: Wallace JW, Mansell RL (eds) Biochemical interaction between plants and insects. Plenum, New York, pp 168–213

    Google Scholar 

  • Ruberson JR, Tauber MJ, Tauber CA, Tingey WM (1989) Interactions at three trophic levels: Edovum puttleri Grissell (Hymenoptera: Eulophidae), the Colorado potato beetle, and insect-resistant potatoes. Can Entomol 121: 841–851

    Google Scholar 

  • Strauss SY (1991) Indirect effects in community ecology: their definition, study and importance. Trends Ecol Evol 6: 206–210

    Google Scholar 

  • Weis AE, Abrahamson WG (1986) Evolution of host-plant manipulation by gall makers: ecological and genetic factors in the Solidago-Eurosta system. Am Nat 127:681–695

    Google Scholar 

  • Whitham TG (1978) Habitat selection by Pemphigus aphids in response to resource limitation and competition. Ecology 59: 1164–1176

    Google Scholar 

  • Whitham TG (1983) Host manipulation of parasites: within-plant variation as a defense against rapidly evolving pests. In: Denno RF, McClure MS (eds) Variable plants and herbivores in natural and managed systems. Academic Press, New York, pp 15–41

    Google Scholar 

  • Whitham TG (1989) Plant hybrid zones as sinks for pests. Science 244: 1490–1493

    Google Scholar 

  • Wilson, D (1995) Fungal endophytes which invade insect galls: insect pathogens, benign saprophytes, or fungal inquilines? Oecologia 103: 255–260

    Google Scholar 

  • Wootton JT (1994) The nature and consequences of indirect effects in ecological communities. Annu Rev Ecol Syst 25: 443–466

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Dickson, L.L., Whitham, T.G. Genetically-based plant resistance traits affect arthropods, fungi, and birds. Oecologia 106, 400–406 (1996). https://doi.org/10.1007/BF00334568

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00334568

Key words

Navigation