Tritrophic Interactions and Insect Behavior

The parasitic wasp, Aphytis melinus, piercing the cover of California red scale, Aonidiella aurantii, and depositing an egg on the scale body beneath the cover.

 

Newly-expanded covers of California red scales removed from their scales to show the body of the scale insect that normally resides beneath the scale cover.

 

An adult female Aphytis melinus ovipositing on a disk of filter paper treated with O-caffeoyltyrosine.

 

I first became interested in the extension of plant-insect interactions to the third trophic level while preparing a review chapter for Variable Plants and Herbivores in Natural and Managed Systems, edited by Robert Denno and Mark McClure. I was particularly intrigued by some early studies suggesting that variation among citrus cultivars my influence a "classical" biological control system involving the California red scale and the introduced parasitoid, Aphytis melinus.

I had the opportunity to work on this system after assuming my present position at UC Riverside. In collaboration with Dr. Robert Luck, we found that, indeed, not all citrus varieties were alike, and the variation in plant quality for growth and survival of California red scale affected the suitability of scale reared on different host plants for utilization by A. melinus. These effects included not only reduced size and fecundity of wasps from scales themselves reared on less-suitable hosts, but also a more male-biased sex ratio. It has long been known that A. melinus has haplodiploid sex determination, and that female wasps allocate the sex of their offspring on the basis of host size. Haploid eggs become male wasps and are allocated to relatively small hosts, while diploid eggs become female wasps and are allocated to relatively large hosts. Thus, if their host scales reach different sizes on different host plants, then the sex ratio of wasps emerging from hosts on different host plants are also expected to differ. This is indeed the case, and we suggested that the capacity of A. melinus to provide effective biological control of California red scale will vary among different citrus cultivars through sex ratio variation.

After showing the life history consequences of hostplant-induced variation in scale quality to A. melinus, our next objective was to determine if scales reared on different host plants differed in their ability to be recognized or accepted by foraging A. melinus females. This objectives was somewhat more difficult to achieve, because we needed to learn how such host recognition and acceptance was mediated chemically.

The structure of O-caffeoyltyrosine, the oviposition stimulant from California red scale covers for Aphytis melinus

We identified a chemical substance in the covers of scales that elicited oviposition probes by A. melinus. This substance, O-caffeoyltyrosine, was a new compound and is a simple ester between the protein amino acid, tyrosine, and caffeic acid. Wasps responded quantitatively to variation in O-caffeoyltyrosine content in the laboratory. We quantified the concentration of O-caffeoyltyrosine in scale covers of field-reared scales and found that scales reared on some of their less suitable plant hosts not only were smaller, but also produced covers with reduced O-caffeoyltyrosine content. These covers also were less attractive to wasps in bioassays. Thus, feeding site selection by California red scale not only directly affects scale survival and growth, but it also indirectly affects the discovery of scales and their utilization by A. melinus: scale crawlers that select feeding sites that maximize their rate of growth are also maximizing their risk of discovery and utilization by A. melinus. We were among the first to show the ecological consequences of quantitative variation in chemicals used by natural enemies for host identification.

An underlying paradigm of tritrophic interactions is that those interactions are evolved. Presumably, natural enemies are agents of selection that favor plants with traits that increase the success of those natural enemies. More successful of natural enemies should then improve plant fitness by reducing losses from herbivores. The association involving citrus cultivars, California red scale, and A. melinus is clearly not an evolved interaction; the variation in plant traits that affect the interaction between California red scale and A. melinus are not the results of natural selection, but merely an inadvertent consequence of plant breeding for agronomic traits that are incidental to the herbivore-parasitoid interaction. Although the study of tritrophic interactions in agricultural systems can provide information about how such interactions function, the evolutionary implications that can be drawn from studies of applied systems are limited.

 

My primary goal is to understand the potential evolution of tritrophic interactions, therefore, I expect that most of my future work on tritrophic interactions will emphasize natural rather than applied systems.  The trichome dimorphism of D. wrightii provides an exciting opportunity to investigate a natural tritrophic interaction because the glandular trichomes that provide a direct benefit by providing resistance to several insect herbivores may also have an indirect cost associated with their production through their deleterious effects on some natural enemies of those herbivores.  Understanding the balance between the direct and indirect costs and benefits of glandular trichome production will be a primary research objective of my laboratory for the next few years.

Publications

  • Gassmann, A. J. and J. Daniel Hare. 2005.  Indirect Cost of a Defensive Trait: Variation in Trichome Type Affects the Natural Enemies of Herbivorous Insects on Datura wrightii.  Oecologia. 144: 62-71. Abstract. Link to Article.
  • Hare, J. Daniel.  2002.  Plant Genetic Variation in tritrophic interactions, pp 8 – 43 in Tscharntke, T. and Hawkins, B. A., editors, Multitrophic Level Interactions.  Cambridge University Press, Cambridge, U. K. PDF
  • Hare, J. Daniel and D. J. W. Morgan. 2000. Chemical conspicuousness of an herbivore to its natural enemy: Effect of feeding site selection. Ecology 81: 509-519.  PDF.
  • Morgan, D. J. W. and J. Daniel Hare. 1998. Volatile cues used by Aphytis melinus for host location: California red scale revisited. Entomologia Experimentalis et Applicata 88: 235-245. Link to Article
  • Morgan, D. J. W. and J. Daniel Hare. 1998. Innate and Learned cues: Scale cover selection by Aphytis melinus (Hymenoptera: Aphelinidae). Journal of Insect Behavior 11:463-479. Link to Article
  • Morgan, D. J. W. and J. Daniel Hare. 1997. Uncoupling physical and chemical cues: The independent roles of scale cover size and kairomone concentration on host selection by Aphytis melinus DeBach (Hymenoptera: Aphelinidae). Journal of Insect Behavior 10:679-694. View
  • Hare, J. Daniel and D. J. W. Morgan. 1997. Mass-Priming Aphytis: Behavioral Improvement of insectary-reared biological control agents. Biological Control 10: 207-214. Link to Article
  • Hare, J. Daniel, D. J. W. Morgan, and T. Nguyun. 1997. Increased parasitization of California red scale in the field after exposing its parasitoid, Aphytis melinus to a synthetic kairomone. Entomologia Experimentalis et Applicata 82: 73-81. Link to Article.
  • Trumble, J. T. and J. Daniel Hare. 1997. "Tritrophic Interactions in the management of Spodoptera exigua on celery," pp 117-134 In Bondari, K. Editor, New Developments in Entomology, Research Signpost, Trivandrum.
  • Hare, J. Daniel. 1996. Priming Aphytis: Behavioral modification of host selection by exposure to a synthetic contact kairomone. Entomologia Experimentalis et Applicata 78: 263-269. Link to Article
  • Berdegue, M., J. T. Trumble, J. Daniel Hare and R. A. Redak. 1996. Is it enemy-free space? - the evidence for terrestrial insects and fresh water arthropods. Ecological Entomology 21: 203-217.
  • Meade, T. and J. Daniel Hare. 1995. Integration of host plant resistance and Bacillus thuringiensis insecticides in the management of lepidopterous pests of celery. Journal of Economic Entomology. 88:1787-1794.
  • Meade, T. and J. Daniel Hare. 1994. Effects of genetic and environmental host plant variation on the susceptibility of two noctuids to Bacillus thuringiensis. Entomologia Experimentalis et Applicata 70: 165-178.  Link to Article.
  • Hare, J. Daniel and R. F. Luck. 1994. Environmental variation in physical and chemical cues used by the parasitic wasp, Aphytis melinus for host recognition. Entomologia Experimentalis et Applicata 72: 97-108.  Link to Article.
  • Hare, J. Daniel, J. G. Millar, and R. F. Luck. 1993. A caffeic acid ester mediates host recognition by a parasitic wasp. Naturwissenschaften 80: 92-94. Link to Article
  • Meade, T., and J. Daniel Hare. 1993. Effects of differential host plant consumption by Spodoptera exigua (Lepidoptera: Noctuidae) on Bacillus thuringiensis efficacy. Environmental Entomology 22: 432-437.
  • Millar, J. G. and J. Daniel Hare. 1993. Identification and synthesis of a kairomone inducing oviposition by the parasitoid Aphytis melinus From California red scale covers. Journal of Chemical Ecology. 19: 1721-1736. Link to Article
  • Navon, A., J. Daniel Hare and B. A. Federici. 1993. Interactions among Heliothis virescens larvae, cotton condensed tannin and the Cry(IA(c) d-endotoxin of Bacillus thuringiensis. Journal of Chemical Ecology 18: 2485-2499.  Link to Article.
  • Hare, J. Daniel. 1992. Effects of Plant Variation on Herbivore-Natural Enemy Interactions. pp 278-298 in R. S. Fritz and E. L. Simms, eds. Plant Resistance to Herbivores and Pathogens: Ecology, Evolution, and Genetics. University of Chicago Press, Chicago, Ill.
  • Hare, J. Daniel and R. F. Luck. 1991. Indirect effects of citrus cultivars on life history parameters of a parasitic wasp. Ecology. 72: 1576-1585.  Link to Article.
  • Hare, J. Daniel, and T. G. Andreadis. 1983. Variation in the susceptibility of Leptinotarsa decemlineata (Coleoptera : Chrysomelidae) when reared on different host plants to the fungal pathogen, Beauveria bassiana in the field and laboratory. Environmental Entomology 12: 1891 - 1896.

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