Skip to main content

Advertisement

Log in

Seasonal shift from bottom-up to top-down impact in phytophagous insect populations

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

Abstract

Although many studies now examine how multiple factors influence the dynamics of herbivore populations, few studies explicitly attempt to document where and when each is important and how they vary and interact. In fact, how temporal variation in top-down (natural enemies) and bottom-up (host plant resources) factors affect herbivore dynamics has been suggested as a particularly important yet poorly understood feature of terrestrial food webs. In this study we examined how temporal changes in predator density (wolf spiders, sheet-web builders, and mirid egg predators) and host-plant resources (plant quality and structural complexity) influence the population dynamics of the dominant phytophagous insects on Atlantic-coast salt marshes, namely Prokelisia planthoppers (Homoptera: Delphacidae). We designed a factorial experiment in meadows of Spartina alterniflora to mimic natural variation in vegetation quality and structure by establishing two levels of plant nutrition (leaf nitrogen content) by fertilization, and two levels of habitat complexity by adding leaf litter (thatch). We then assessed seasonal changes in the strength of bottom-up (plant quality) and top-down (predator) impacts on planthopper populations. Planthopper populations responded positively to increased plant quality treatments in late summer. Despite the greater number of planthopper adults colonizing fertilized Spartina plots compared to unfertilized controls, the offspring of these colonists were much less abundant at the end of the season in fertilized plots, particularly those with thatch. The initial colonization effect was later erased because arthropod predators selectively accumulated in fertilized plots where they inflicted significant mortality on all stages of planthoppers. Predators rapidly colonized fertilized plots and reached high densities well in advance of planthopper colonization, a response we attribute to their rapid aggregation in complex-structured habitats with readily available alternative prey. Our results suggest that plant resources not only mediate the strength of predator impacts on herbivore populations, but they also promote the coupling of predator and prey populations and thus influence when enemy impacts are realized.

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.

Fig. 1A–C.
Fig. 2A–D.
Fig. 3.

Similar content being viewed by others

References

  • Bottrell DG, Barbosa P, Gould F (1998) Manipulating natural enemies by plant variety selection and modification: a realistic strategy? Annu Rev Entomol 43:347–367

    Article  CAS  Google Scholar 

  • Boyer KE, Zedler JB (1996) Damage to cordgrass by scale insects in a constructed salt marsh: effects of nitrogen additions. Estuaries 19:1–12

    CAS  Google Scholar 

  • Bultman TL, Uetz GW (1982) Abundance and community structure of forest floor spiders following litter manipulation. Oecologia 55:34–41

    Google Scholar 

  • Campbell BC, Duffey SS (1979) Tomatine and parasitic wasps: potential incompatibility of plant antibiosis with biological control. Science 205:700–702

    CAS  Google Scholar 

  • Cook A, Denno RF (1994) Planthopper/plant interactions. In: Denno RF, Perfect TJ (eds) Planthoppers: their ecology and management. Chapman and Hall, New York, pp 114–139

    Google Scholar 

  • Denno RF (1983) Tracking variable host plants in time and space. In: Denno RF, McClure MS (eds) Variable plants and herbivores in natural and managed systems. Academic Press, New York, pp 291–341

  • Denno RF (1994) Life history variation in planthoppers. In: Denno RF, Perfect TJ (eds) Planthoppers: their ecology and management. Chapman and Hall, New York, pp 163–215

    Google Scholar 

  • Denno RF, Grissell EE (1979) The adaptiveness of wing-form dimorphism in the salt-marsh inhabiting planthopper, Prokelisia marginata (Homoptera: Delphacidae). Ecology 60:221–236

    Google Scholar 

  • Denno RF, Peterson MA (2000) Caught between the devil and the deep blue sea, mobile planthoppers escape natural enemies and locate favorable host plants. Am Entomol 46:95–109

    Google Scholar 

  • Denno RF, Raupp MJ, Tallamy DW, Reichelderfer CF (1980) Migration in heterogeneous environments: differences in habitat selection between the wing forms of the dimorphic planthopper, Prokelisia marginata (Homoptera: Delphacidae). Ecology 61:859–867

    Google Scholar 

  • Denno RF, Douglass LW, Jacobs D (1986) Effects of crowding and host plant nutrition on the development and body size of the wing-dimorphic planthopper Prokelisia marginata. Ecology 67:116–123

    Google Scholar 

  • Denno RF et al. (1996) Habitat persistence underlies intraspecific variation in the dispersal strategies of planthoppers. Ecol Monogr 64:389–408

    Google Scholar 

  • Denno RF, Gratton C, Peterson MA, Langellotto GA, Finke DL, Huberty AF (2002) Bottom-up forces mediate natural-enemy impact in a phytophagous insect community. Ecology 83:1443–1458

    Google Scholar 

  • Dicke M, Sabelis MW (1988) How plants obtain predatory mites as bodyguards. Neth J Zool 38:148–165

    Google Scholar 

  • Döbel HG, Denno RF (1994) Predator-planthopper interactions. In: Denno RF, Perfect TJ (eds) Planthoppers: their ecology and management. Chapman and Hall, New York, pp 325–399

    Google Scholar 

  • Döbel HG, Denno RF, Coddington JA (1990) Spider (Araneae) community structure in an intertidal salt marsh: effects of vegetation structure and tidal flooding. Environ Entomol 19:1356–1370

    Google Scholar 

  • English-Loeb G, Norton AP, Gadoury DM, Seem RC, Wilcox WF (1999) Control of powdery mildew in wild and cultivated grapes by a tydeid mite. Biol Control 14:97–103

    Article  Google Scholar 

  • Ernest SKM, Brown JH, Parmenter RR (2000) Rodents, plants, and precipitation: spatial and temporal dynamics of consumers and resources. Oikos 88:470–482

    Google Scholar 

  • Espelie KE, Bernays EA, Brown JJ (1991) Plant and insect cuticular lipids serve as behavioral cues for insects. Arch Insect Biochem Physiol 17:223–233

    CAS  Google Scholar 

  • Finke DL, Denno RF (2002) Intraguild predation diminished in complex-structured vegetation: implications for prey suppression. Ecology 83:643–653

    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 

  • Halaj J, Cady AB, Uetz GW (2000) Modular habitat refugia enhance generalist predators and lower plant damage in soybeans. Environ Entomol 29:383–393

    Google Scholar 

  • Hallander H (1970) Prey, cannibalism and microhabitat selection in the wolf spiders Pardosa chelata O.F. Mueller and P. pullata Clerck. Oikos 21:337–340

    Google Scholar 

  • Hartvigsen G, Wait DA, Coleman JS (1995) Tri-trophic interactions influenced by resource availability: predator effects on plant performance depend on plant resources. Oikos 77:463–468

    Google Scholar 

  • Holt RD (2000) Trophic cascades in terrestrial ecosystems. Reflections on Polis et al. Trends Ecol Evol 15:444–445

    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 

  • Hunter MD, Varley GC, Gradwell GR (1997) Estimating the relative roles of top-down and bottom-up forces on insect herbivore populations: a classic study revisited. Proc Natl Acad Sci USA 94:9176–9181

    Google Scholar 

  • Huxel GR, McCann K (1998) Food web stability: the influence of trophic flows across habitats. Am Nat 152:460–469

    Article  Google Scholar 

  • Kareiva P (1987) Habitat fragmentation and the stability of predator-prey interactions. Nature 326:388–390

    Google Scholar 

  • Kareiva P, Sahakian R (1990) Tritrophic effects of a simple architectural mutation in pea plants. Nature 345:433–434

    Google Scholar 

  • Kato M (1994) Alternation of bottom-up and top-down regulation in a natural population of an agromyzid leafminer, Chromatomyia suikazurae. Oecologia 97:9–16

    Google Scholar 

  • Kauffman WC, Kennedy GG (1989) Relationship between trichome density in tomato and parasitism of Heliothis spp. (Lepidoptera: Noctuidae) eggs by Trichogramma spp. (Hymenoptera: Trichogrammatidae). Environ Entomol 18:698–704

    Google Scholar 

  • Landis D, Wratten SD, Gurr GM (2000) Habitat management to conserve natural enemies of arthropod pests in agriculture. Annu Rev Entomol 45:175–201

    Article  CAS  PubMed  Google Scholar 

  • Langellotto GA (2002) Aggregation of invertebrate predators in complex-structured habitats: role of altered cannibalism, intraguild predation, prey availability, and microclimate, Ph.D. dissertation. Department of Entomology. University of Maryland, College Park, Md., p 208

  • Lasalle MW, Delacruz AA (1985) Seasonal abundance and diversity of spiders in 2 intertidal marsh plant communities. Estuaries 8:381–393

    Google Scholar 

  • Lawton JH, McNeill S (1979) Between the devil and the deep blue sea: on the problem of being a herbivore. In: Anderson RM, Turner BD, Taylor LR (eds) Population dynamics. Symp Br Ecol Soc 20:223–244

    Google Scholar 

  • Marples TG (1966) A radionucleotide tracer study of arthropod food chains in a Spartina salt marsh ecosystem. Ecology 47:270–277

    Google Scholar 

  • Nakano S, Miyasaka H, Kuhara N (1999) Terrestrial-aquatic linkages: riparian arthropod inputs alter trophic cascades in a stream food web. Ecology 80:2435–2441

    Google Scholar 

  • Oksanen L, Fretwell S, Arruda J, Niemela P (1981) Exploitation ecosystems in gradients of primary production. Am Nat 118:240–261

    Article  Google Scholar 

  • Olmstead KL, Denno RF, Morton TC, Romeo JT (1997) Influence of Prokelisia planthoppers on amino acid composition and growth of Spartina alterniflora. J Chem Ecol 23:303–321

    CAS  Google Scholar 

  • Ostfeld RS, Keesing F (2000) Pulsed resources and community dynamics of consumers in terrestrial ecosystems. Trends Ecol Evol 15:232–237

    PubMed  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, Hurd SD, Jackson CT, Sanchez-Piñero F (1998) Multifactor population limitation: variable spatial and temporal control of spiders on Gulf of California islands. Ecology 79:490–502

    Google Scholar 

  • Power ME (1992) Top-down and bottom-up forces in food webs: do plants have primacy? Ecology 73:733–746

    Google Scholar 

  • Power ME, Parker MS, Wootton JT (1996) Disturbance and food chain length in rivers. In: Polis GA, Winemiller KO (eds) Food webs. Chapman and Hall, New York, pp 286–297

  • Price PW, Bouton CE, Gross P, McPheron BA, Thompson JN, Weis AE (1980) Interactions among three trophic levels: influence of plants on interactions between insect herbivores and natural enemies. Annu Rev Ecol Syst 11:41–65

    Google Scholar 

  • Reichert SE, Bishop L (1990) Prey control by an assemblage of generalist predators: spiders in garden test systems. Ecology 71:1441–1450

    Google Scholar 

  • SAS Institute (2000) JMP, ver. 4.0.4. SAS Institute, Cary, N.C.

  • Scheu S (2001) Plants and generalist predators as links between the below-ground and above ground system. Basic Appl Ecol 2:3–13

    Google Scholar 

  • Settle WH et al. (1996) Managing tropical rice pests through conservation of generalist natural enemies and alternative prey. Ecology 77:1975–1988

    Google Scholar 

  • Takabayashi J et al. (1998) Plant effects on parasitoid foraging: differences between two tritrophic systems. Biol Control 11:97–103

    Article  Google Scholar 

  • Treacy MF, Benedict JH, Segers JC, Morrison RK, Lopez JD (1986) Role of cotton trichome density in bollworm (Lepidoptera: Noctuidae) egg parasitism. Environ Entomol 15:365–368

    Google Scholar 

  • Turlings TCJ, Tumlinson JH, Lewis WJ (1990) Exploitation of herbivore-induced plant odors by host-seeking parasitic wasps. Science 250:1251–1253

    CAS  Google Scholar 

  • Turlings TCJ, Bernasconi M, Bertossa R, Bigler F, Caloz G, Dorn S (1998) The induction of volatile emissions in maize by three herbivore species with different feeding habits: possible consequences for their natural enemies. Biol Control 11:122–129

    Article  Google Scholar 

  • Vince SW, Valiela I, Teale JM (1981) An experimental study of the structure of herbivorous insect communities in a salt marsh. Ecology 62:1662–1678

    Google Scholar 

  • von Ende CN (1993) Repeated-measures analysis: growth and other time-dependent measures. In: Scheiner SM, Gurevitch J (eds) Design and analysis of ecological experiments. Chapman and Hall, New York, pp 113–137

  • Walker M, Jones TH (2001) Relative roles of top-down and bottom-up forces in terrestrial tritrophic plant-insect herbivore-natural enemy systems. Oikos 93:177–187

    Google Scholar 

Download references

Acknowledgments

Mark Hunter, David Wise, Deborah Finke and two anonymous reviewers read earlier drafts of this manuscript and we hope to have incorporated their many insightful suggestions. Ken Able and Bobbie Zlotnik of the Rutgers University Marine Station facilitated our research at the Tuckerton field site. We are most grateful to these colleagues for their advice and support. This research was supported by National Science Foundation Grants DEB-9527846 and DEB-9903601 to RFD.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Claudio Gratton.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Gratton, C., Denno, R.F. Seasonal shift from bottom-up to top-down impact in phytophagous insect populations. Oecologia 134, 487–495 (2003). https://doi.org/10.1007/s00442-002-1137-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-002-1137-8

Keywords

Navigation