Herbivory

1. Herbivory Peter B. McEvoy Ent 420/520 Insect Ecology

2. Outline • Plants as food and habitat for insects • Effects of plants on insect populations • Food quantity • Food quality • Complex patterns of spatial and temporal correlation • Effects of insects on plant populations • Coevolution • Plant resistance strategies • Integrated pest management • Biological control of weeds • Trophic structure of ecosystems

3. Asymmetry in Insect-plant Relationship Phytophagous Insect Ecology Crawley Evolution Jermy Plant

4. Plant-herbivore Interactions(Crawley 1983) • Asymmetry in plant-herbivore interactions: plants have more impact on herbivores than herbivores have on plants • Differences between vertebrate and invertebrate herbivores. Mammalian are often food limited, yet insect herbivores are seldom food limited and often regulated by predators, parasites and diseases • Insect herbivore effects on plants: Evidence of absence or absence of evidence?

5. Pipevine Swallowtail Battus philenor on Aristolochia • Effect of plant on insect. Why does ovipositional host preference change seasonally from Aristolochiareticulata to A. serpentaria? (Rausher 1981) • Effect of insect on plant. What is the effect of herbivory on lifetime reproductive success of A. reticulata, a long-lived perennial, iteroparous plant? (Rausher and Feeny 1980)

6. Swallowtail Case StudyEvidence Excluding Predation

7. Swallowtail Case StudyEvidence Favoring Host Quality Faster growth on younger leaves related to higher [N]; N as an appropriate “currency” for modeling insect growth Faster growth on younger leaves; distinguishing preference from suitability as a cause of slow growth Relative Growth Rate (RGR) Relative Consumption Rate (RCR) Relative Consumption Rate N (RCRN)

8. Effects of Plants on InsectsSummary of Evidence • No seasonal increase in proportion of larvae that disappear from A. reticulata due to predation • Seasonal decrease in acceptability of foliage • Seasonal decline in amount of young foliage • Faster growth on young foliage • Young foliage more suitable due to higher [N] • Sclerophylly (leaves of low nutrient and higher fiber content) as a “plant defense”

9. Plant Quality and Larch Bud Moth Performance Pupal weight decreases with fiber content of needles Larval mortality increases with fiber content of needles

10. Food Quality and Larch Bud Moth Dynamics

11. “Vaccinating” Grape Vines Against Spider Mites (Karban) Virulent Pacific spider mite (above) and benign Willamette mite (below)

12. Summary of Effects of Plants on Insects • Consumer-resource relationship influenced by both quantity and quality of food resources • Plant Quality related to nitrogen, water, tissue toughness, secondary chemicals • Changes in Plant Quality invoked in explanations of insect population dynamics • Manipulating plant quality for pest control

13. Are plant populations seed-limited? Turnbull, L. A., M. J. Crawley, and M. Reese. 2000. Are plant populations seed-limited? A review of seed sowing experiments. Oikos 88:225-238. • Definition. They define seed limitation to be an increase in population size following seed addition. • Two types of experiments. They review two types of seed addition experiments: seed augmentation studies where seeds are added to existing populations; and seed introductions where seeds are sown in unoccupied sites. • Overall results. Approximately 50% of seed augmentation experiments show evidence of seed limitation. These studies show that seed limitation tends to occur more commonly in early successional habitats and in early successional species.

14. Protocol recommended for seed addition experimentsmodified from Turnbull et al. 2000 • Estimate seed output of natural population. Facilitate comparison by making seed addition some specified multiple of natural seed rain. • Manipulate seed outputs over a sufficient range. • Monitor response throughout the life cycle, at least to adult stage. • Manipulate seed-feeding herbivores as part of the design. Combine enhanced, control, and diminished seed predators with enhanced, control, and diminished seed rain. • Conduct additions on appropriate spatial and temporal scale. Mimic the spatail and temporal scale "sampled" by the life history of the organism.

15. Models of plant recruitmentOutcome of seed addition depends on which model applies • Hierarchical ranking of competitors • Fixed hierarchy • Variable hierarchy • Lottery Model – juveniles chosen at random from pool of potential recruits

16. Seed limitation more common in early successional habitats

17. Seed limitation more common in early successional species (confounded with habitat)

18. Effects of Insects on Reproductive Success of Cirsium canescens • Removal experiment: insecticide Herbivore effect = protected – exposed • Spatial,temporal, organizational scales of observation • Temporal scales (within and between years) • Spatial scales (region, habitat, between plant, within plant) • Organizational scales (plant/arthropod association, guild, and species within guild • Platte thistle inflorescence feeders • Tephritid flies Orelliaoccidentalis and Paracantha culta • Pyralid moth Hoemosoma stypetallum

19. Life Cycle Graph for Thistle

20. Seedling Shadows

21. Effects Conditional on Year and Habitat

22. Lifetime Maternal Fitness in Protected and Exposed Plants (Louda and Potvin 1984)

23. Swallowtail Case StudyEffects of Insects on Plant Populations • Growth. Insects affect how plants grow • Reproduction. Plant growth linked to reproduction • Basis for extrapolation to longer time scales. Projecting growth and reproduction of exposed and protected plants from matrices

24. Factorial ExperimentPlant Density x Herbivory No measures of temporal and spatial variability in herbivore effects, which are assumed to be representative of average values

25. Projecting Growth of Protected and Exposed Plants

26. Growth Matrices Exposed Plants Protected Plants For protected plants, elements below the diagonal tend to be large, while those above the diagonal tend to be small, indicating that for protected plants, there are many more plants that increase in size than decrease. For exposed plants, the reverse is true.

27. Projected Growth for Protected and Exposed Plants

28. Projected Seed Production for Protected and Exposed Plants

29. Effects of Insect Herbivores on Natural Communities and Their Role As Agents of Natural SelectionShortcomings of Plant-insect Literature • Temporal scale is too brief • Spatial scale is too small • Organizational scale too limited • Focus on crops or introduced weeds lacking a full complement of natural enemies • Methodological flaws such as inadequate controls or unwanted side effects of manipulation

30. Major Themes • Insect herbivores rarely limited by their food supply • Reports of devastating impacts of insect herbivores come from crops and biocontrol of weeds, situations where herbivore’s natural complement of enemies may be absent or ineffective

31. Effects of Insects on Plant Succession in ‘Natural’ Communities • Primary succession • On lupine after eruption of Mt St Helens in NA (Fagan & Bishop 2000) • Leaf beetles on willow in sand dunes in NA (Bach) • Secondary succession • Spittlebugs in early old field succession in NA (Carson and Root 1999) • Leaf beetles in later old field succession in NA (Carson and Root 2000) • Foliage- and root-feeding insects in old field succession in UK (Brown et al)

32. Herbivore effects on primary succession on Mt St Helens

33. Goldenrod Fauna • 103 species.103 species complete “substantial portion of development” on this plant. Includes varying phenologies, feeding styles, host ranges, and tactics for escaping enemies. • 42 spp specialists.42 species in 17 separate families are specialists on Solidago and a few related genera • A few large effects or many small?A few insects species (<10 of 103 spp) account for most of the herbivore load in survey – a leaf chewer (chrysomelid Microrhopala vittata) and a sap-tapper (tingid bug Corythucha marmorata) predominate in experiment. Other spp. Individually and collectively “inconsequential” • Genetic variation in “host resistance”.Local populations contain clones that show genetic variation in susceptibility to various suites of herbivores • Genetic variation in “insect virulence”?

34. Goldenrod Sample Across 22 Sites and 6 Yr

35. What Are Your Expectations? • Distribution of species among higher taxa • Distribution of species among functional groups • Distribution of abundance/biomass among species • Differences in per capita effect among stages and species • Patterns in fluctuations of populations • Among species within a site • Within species across sites

36. Schedule of Insecticide Applications

37. Trends in Removal Experiment Shorter stems Fewer flowering plants Underestimate?

38. Logical Approach • Relationship between plant performance and herbivore load • Distribution of herbivore loads across 22 sites and 6 years • Contribution of each insect species to herbivore load • Per capita effects of herbivore species

39. Plant Performance Decreases With Increasing Herbivore Load • Beyond p-values • Models? • Unstable variance? • Estimates of parameters? • Magnitudes of effects? • Biological significance vs. statistical significance? • Suitable transformations? • Conclusions about functional form of the relationships? Mean and variance. Lowering the ceiling on variance

40. Variation in Total Herbivore Loads on Solidago altissima

41. Dominance Increases With Herbivore Load Beetles Trirhabda (10) and Microrhopala (9) dominate survey, Microrhopala and tingid Corythucha dominate experiment

42. Comparing Leaf-chewer and Sap-Tapper Damage (Meyer) For several measures of plant performance…. Per capita effect of spittlebugs (sap tapper) is greater than that of beetles (leaf chewer) (steeper slopes)

43. Excluding Insects With an Insecticide • Selectivity.What about endophages (Gall-making and stem-boring) escaped contact with insecticide? Assume to be random? Why not measure internal feeding by external symptoms? e.g. ball-gall • Timing.Spray scheduleallows for reinfestation by immigration between sprays • Side effects and possible use of “placebo” to counter them • Phyto-toxic effects. • Fertilizing effects.Stimulate plant growth by adding nutrients or water

44. Points Raised by prior class… • Active voice in scientific writing • Issue of a reader’s trust in an author • Long-winded prose?Can field ecology be short and sweet? • Combination of Observational and Experimental Approaches an unreliable basis for extrapolation • Missing relevant detail: diagram layout, graph weather data • Randomization as a remedyfor coping with uncontrolled, possible influence variables(soils, genotypes, etc. etc.) • Overlooks possible unwanted side effects of insecticide • Include a placebo, publish greenhouse assay, check for drift • May disrupt regulation of herbivore populations by natural enemies • May increase resistant endophages • Unanticipated effects of destructive harvest of inflorescences and seeds • Possibly Combining Nondestructive vs Destructive Harvest

45. More Points Raised by Prior Class… • What is plant vigor? General issue of operational measures • Calculating herbivore loadsassumes other things (guilds, individuals, etc) are all equal, and other things seldom are • Possible unanticipated treatment effectstreatment in one year makes plants more attractive than control in next? • Local study yield local resultsbut what about the regional study of pattern 22 sites x 6 yr? • Standardize timing of sampling to physiological time: but note his use of insect development as bioindicator • Sampling twice per year is not enough? • Standard sampling vs adaptive sampling –keep everything the same across time and space or modify as you learn • Independence of experimental units • Timing.Spray scheduleallows for re-infestation by immigration between sprays

46. Still more points (tough crowd!)… • Good intentions no substitute for good evidence --too many unpublished studies or mere verbal reassurances addressing unsettled points like abundance of gall formers, unwanted side effects of pesticide • Distance between cause (herbivore load) and effect (plant performance)is great due to possible effects of pesticides on host plant, pesticide-resistant herbivores, below-ground herbivores, non-insect herbivores, weather, and timing of the census

47. Vote for the best quote… • “The difficulties associated with sustaining interest and funding while investigating situations were little is happening probably have a profound effect on our view of nature.” • “Taking all of these observations together, it would appear that food supply very rarely limits the populations of most goldenrod-feeding insects. How this is accomplished, for so many species with such different attributes and enemies, remains an enigma.”

48. Points you might have raised… • Idiosyncratic measures of dependent variables (stem length, stem density, proportion of stems that bloomed, inflorescence mass) and independentvariables (herbivore load) • What is an individual?Ignores distinction between fates of ramets and genets • Empirical study overlooks modelsthat might create a more reliable basis for comparison, interpolation, extrapolation • Experimental units are not strictly independent-they share a species pool of herbivores and natural enemies that is perhaps reduced by insecticide

49. Storage Effect (Chesson) • Fluctuating herbivore pressure • Storage effect.Gains in favorable years stored in invulnerable stage during unfavorable period and contribute to reproduction when favorable conditions return • Assimilate stored in perennial roots • Seeds stored in buried seed pool • Buds stored in buried bud bank • None of which was measured in this study!

50. Herbivore effects on primary succession on Mt St Helens