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Quality or quantity: the direct and indirect effects of host plants on herbivores and their natural enemies

  • Plant Animal Interactions
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Abstract

Resource quality (plant nitrogen) and resource quantity (plant density) have often been argued to be among the most important factors influencing herbivore densities. A difficulty inherent in the studies that manipulate resource quality, by changing nutrient levels, is that resource quantity can be influenced simultaneously, i.e. fertilized plants grow more. In this study we disentangled the potentially confounding effects of plant quality and quantity on herbivore trophic dynamics by separately manipulating nutrients and plant density, while simultaneously reducing pressure from natural enemies (parasitoids) in a fully factorial design. Plant quality of the sea oxeye daisy, Borrichia frutescens, a common coastal species in Florida, was manipulated by adding nitrogen fertilizer to increase and sugar to decrease available nitrogen. Plant density was manipulated by pulling by hand 25 or 50% of Borrichia stems on each plot. Because our main focal herbivore was a gall making fly, Asphondylia borrichiae, which attacks only the apical meristems of plants, manipulating plant nitrogen levels was a convenient and reliable way to change plant quality without impacting quantity because fertilizer and sugar altered plant nitrogen content but not plant density. Our other focal herbivore was a sap-sucker, Pissonotus quadripustulatus, which taps the main veins of leaves. Parasitism of both herbivores was reduced via yellow sticky traps that caught hymenopteran parasitoids. Plant quality significantly affected the per stem density of both herbivores, with fertilization increasing, and sugar decreasing the densities of the two species but stem density manipulations had no significant effects. Parasitoid removal significantly increased the densities of both herbivores. Top-down manipulations resulted in a trophic cascade, as the density of Borrichia stems decreased significantly on parasitoid removal plots. This is because reduced parasitism increases gall density and galls can kill plant stems. In this system, plant quality and natural enemies impact per stem herbivore population densities but plant density does not.

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References

  • Cornell HV, Hawkins BA (1995) Survival patterns and mortality sources of herbivorous insects: some demographic trends. Am Nat 145:563–593

    Article  Google Scholar 

  • Cornell HV, Hawkins BA et al (1998) Towards an empirically-based theory of herbivore demography. Ecol Entomol 23:340–349

    Article  Google Scholar 

  • Dial R, Roughgarden J (1995) Experimental removal of insectivores from rain forest canopy: direct and indirect effects. Ecology 76:1821–1834

    Google Scholar 

  • Dyer LA, Letourneau DK (1999) Trophic cascades in a complex terrestrial community. Proc Natl Acad Sci USA. 96:5072–5076

    Article  CAS  PubMed  Google Scholar 

  • Faeth SH (1994) Induced plant responses: effects on parasitoids and other natural enemies of phytophagous insects. In: Hawkins BA, Sheehan W (eds) Parasitoid community ecology. Oxford University Press, Oxford, pp 245–260

    Google Scholar 

  • Forkner RE, Hunter MD (2000) What goes up must come down? Nutrient addition and predation pressure on oak herbivores. Ecology 81:1588–1600

    Google Scholar 

  • Gomez JM, Zamora R (1994) Top-down effects in a tritrophic system: parasitoids enhance plant fitness. Ecology 75:1023–1030

    Google Scholar 

  • Gratton C, Denno RF (2003) Inter-year carryover effects of a nutrient pulse on Spartina plants, herbivores and natural enemies. Ecology 84:2692–2707

    Google Scholar 

  • Hairston NG, Smith FE et al (1960) Community structure, population control, and competition. Am Nat 44:421–425

    Article  Google Scholar 

  • Halaj J, Wise DH (2001) Terrestrial trophic cascades: how much do they trickle? Am Nat 157:262–281

    Article  Google Scholar 

  • Hawkins BA, Cornell HV et al (1997) Predators, parasitoids and pathogens as mortality agents in phytophagous insect populations. Ecology 78:2145–2152

    Google Scholar 

  • Hunter MD (2001) Multiple approaches to estimating the relative importance of top-down and bottom-up forces on insect populations: experiments, life tables, and time-series analysis. Basic Appl Ecol 4:293–310

    Google Scholar 

  • Hunter MD, Price PW (1992) Playing chutes and ladders: heterogeneity and the relative roles of bottom-up and top-down forces in natural communities. Ecology 73:724–732

    Google Scholar 

  • Jonasson S, Vestergaard et al (1996a) Effects of carbohydrate amendments on nutrient partitioning, plant and microbial performance of a grassland shrub ecosystem. Oikos 75:220–226

    Google Scholar 

  • Jonasson S, Michelsen A et al (1996b) Microbial biomass, C, N and P in two ostic soils and responses to addition of NPK fertilizer and sugar: complications for plant nutrient uptake. Oecologia 106:507–515

    Article  Google Scholar 

  • Karieva P (1983) Influence of vegetation texture on herbivore populations: resource concentration and herbivore movement. In: Denno RF, McClure MS (eds) Variable plants and herbivores in natural and managed systems. Academic, New York, pp 259–289

    Google Scholar 

  • Letourneau DK, Dyer LA (1998) Experimental test in lowland tropical rain forest shows topdown effects through four trophic levels. Ecology 79:1678–1687

    Google Scholar 

  • Luginbill P, McNeil F (1958) Influence of seedling density and row spacings on the resistance of spring wheats to the wheat stem sawfly. J Econ Entomol 51:804–808

    Google Scholar 

  • Machinski J, Whitham TG (1989) The continuum of plant responses to herbivory: the influence of plant association, nutrient availability and timing. Am Nat 134:1–19

    Article  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 

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

    Article  Google Scholar 

  • Mayse M (1978) Effects of spacing between rows on soya bean arthropod populations. J Anim Ecol 15:439–450

    Google Scholar 

  • McNeil S, Southwood TRE (1978) The role of nitrogen in the development of insect/plant relationships. In Harbone JB (ed) Biochemical aspects of plant and animal coevolution. Academic, London, pp 77–89

    Google Scholar 

  • van der Meijden E, Klinkhamer PGL (2000) Conflicting interests of plants and the natural enemies of herbivores. Oikos 89:202–208

    Google Scholar 

  • Michelsen A, Graglia E et al (1999) Different responses of grass and a dwarf shrub to long-term changes in soil microbial biomass, C, N and P following factorial addition of NPK fertilizer, fungicide, and labile carbon to heath. New Phytol 143:523–538

    Article  Google Scholar 

  • Moon DC, Stiling P (2000) Relative importance of abiotically induced direct and indirect effects on a salt marsh herbivore. Ecology 81:470–481

    Google Scholar 

  • Moon DC, Stiling P (2002a) The effects of salinity and nutrients on a tritrophic salt marsh system. Ecology 83:2465–2476

    Google Scholar 

  • Moon DC, Stiling P (2002b) Top-down, bottom-up, or side to side? Within-trophic-level interactions modify trophic dynamics of a salt marsh herbivore. Oikos 98:480–490

    Article  Google Scholar 

  • Moon DC, Stiling P (2002c) The influence of species identity and herbivore feeding mode on top-down and bottom-up effects in a saltmarsh system. Oecologia 133:243–253

    Article  Google Scholar 

  • Moon DC, Stiling P (2003) The influence of legacy effects and recovery from perturbations in a tri-trophic saltmarsh complex. Ecol Entomol 28:457–466

    Article  Google Scholar 

  • Pace ML, Cole JJ et al (1999) Trophic cascades revealed in diverse ecosystems. Trends Ecol Evol 14:483–488

    Article  PubMed  Google Scholar 

  • Parry D, Herms DA et al (2003) Responses of an insect folivore and its parasitoids to multi year experimental defoliation of aspen. Ecology 84:1768–1783

    Google Scholar 

  • Persson L (1999) Trophic cascades: abiding heterogeneity and the trophic level concept at the end of the road. Oikos 85:385–397

    Google Scholar 

  • Polis GA (1999) Why are parts of the world green? Multiple factors control productivity and the distribution of biomass. Oikos 86:3–15

    Google Scholar 

  • Polis GA, Strong DR (1996) Food web complexity and community dynamics. Am Nat 147:813–846

    Article  Google Scholar 

  • Polis GA, Sears ALW et al (2000) When is a trophic cascade a trophic cascade? Trends Ecol Evol 15:473–475

    Article  PubMed  Google Scholar 

  • Price PW, Bouton CE et al (1980) Interactions among three trophic levels: influence of plants on interactions between herbivores and natural enemies. Annu Rev Ecol Syst 11:41–65

    Article  Google Scholar 

  • Pringle CM, Hamazaki T (1997) Effects of fishes on algal response to storms in a tropical stream. Ecology 78:2432–2442

    Google Scholar 

  • Rhiands M, English-Loeb G (2003) Testing the resource concentration hypothesis with tarnished plant bug on strawberry: density of hosts and patch size influence the interaction between abundance of nymphs and incidence of damage. Ecol Entomol 28:348–358

    Article  Google Scholar 

  • Root RB (1973) Organization of a plant-arthropod association in simple and diverse habitats: the fauna of collards (Brassica oleracea) . Ecol Monogr 43:95–124

    Google Scholar 

  • Rossi AM, Stiling P (1995) Interspecific variation in growth rate, gall size, and parasitism of galls induced by Asphondylia borrichiae. Ann Entomol Soc Am 88:39–44

    Google Scholar 

  • Rossi AM, Stiling PD et al (1992) Does gall diameter affect the parasitism rate of Asphondylia borrichiae (Diptera: Cecidomyiidae)? Ecol Entomol 17:149–154

    Google Scholar 

  • Schmidt IK, Michelsen A et al (1997) Effects on plant production after addition of labile carbon to arctic/alpine soils. Oecologia 112:305–313

    Article  Google Scholar 

  • Schmitz OJ, Hambaeck PA, Beckerman AP (2000) Trophic cascades in terrestrial systems: a review of the effects of carnivore removals on plants. Am Nat 155:141–153

    Article  PubMed  Google Scholar 

  • Shaver GR, Chapin III FS (1980) Response to fertilization by various plant growth forms in an Alaskan tundra: nutrient accumulation and growth. Ecology 61:662–675

    CAS  Google Scholar 

  • Slansky F Jr, Rodriguez JG (eds) (1987) Nutrition ecology of insects, mites, spiders and related invertebrates. Wiley, New York

    Google Scholar 

  • Stiling P, Rossi AM (1996) Complex interactions of genotype and environment on insect herbivores and their enemies. Ecology 77:2212–2218

    Google Scholar 

  • Stiling P, Rossi AM (1997) Experimental manipulations of top-down and bottom-up factors in a tri-trophic system. Ecology 78:1602–1606

    Google Scholar 

  • Stiling PD, Throckmorton A et al (1991) Biology and rates of parasitism of the salt-marsh-inhabiting planthoppers Prokelisia marginata and P. dolus. Florida Entomologist 74:81–87

    Google Scholar 

  • Stiling P, Rossi AM et al (1999) Weak competition between coastal insect herbivores. Florida Entomol 82:599–608

    Google Scholar 

  • Strong DR (1992) Are trophic cascades all wet? Differentiation and donor-control in speciose ecosystems. Ecology 73:747–754

    Google Scholar 

  • Turlings TCJ, Loughgrin JH et al (1995) How caterpillar-damaged plants protect themselves by attracting parasitic wasps. Proc Natl Acad Sci USA 92:4169–4174

    CAS  PubMed  Google Scholar 

  • Turner J, Olsen PR (1976) Nitrogen relations in a Douglas fir plantation. Ann Bot 40:1185–1193

    CAS  Google Scholar 

  • Wallace JB, Eggert SL et al (1997) Multiple trophic levels of a forest stream linked to terrestrial litter inputs. Science 277:102–104

    Article  CAS  Google Scholar 

  • Waring GL, Cobb NS (1992) The impact of plant stress on herbivore population dynamics. In: Bernays E (ed) Insect-plant interactions, vol 4. CRC, Boca Raton , pp 168–226

  • White TCR (1978) The importance of a relative shortage of food in animal ecology. Oecologia 33:71–86

    Google Scholar 

  • Wooton JT, Power ME (1993) Productivity, consumers, and the structure of a river food chain. Proc Natl Acad Sci USA 90:1384–1387

    PubMed  Google Scholar 

  • Wooton JT, Parker MS et al (1996) Effects of disturbance on river food webs. Science 273:1558–1561

    Google Scholar 

Download references

Acknowledgements

This research was funded by NSF grant DEB 00-89226. Thanks to Robert Browning and Jim Wilson at Fort DeSoto Park for access to field sites. Thanks also to Heidi Hughes, Stephanie Morse, and Lori Thompson for valuable assistance in the field. Jim Cronin provided valuable criticism of the manuscript. The experiments outlined in this paper comply with the current laws of the USA.

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Stiling, P., Moon, D.C. Quality or quantity: the direct and indirect effects of host plants on herbivores and their natural enemies. Oecologia 142, 413–420 (2005). https://doi.org/10.1007/s00442-004-1739-4

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