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Ecological Research

, Volume 21, Issue 1, pp 26–34 | Cite as

Bottom-up trophic cascades and material transfer in terrestrial food webs

  • Hideki Kagata
  • Takayuki Ohgushi
Special Feature Relationships between biodiversity and ecosystem functioning across different scales

Abstract

In contrast to top-down trophic cascades, few reviews have appeared of bottom-up trophic cascades. We review the recent development of research on bottom-up cascades in terrestrial food webs, focusing on tritrophic systems consisting of plants, herbivorous insects, and natural enemies, and attempt to integrate bottom-up cascade and material transfer among trophic levels. Bottom-up cascades are frequently reported in various tritrophic systems, and are important to determine community structure, population dynamics, and individual performance of higher trophic levels. In addition, we highlight several features of bottom-up cascades. Accumulation or dilution of plant nutritional and defensive materials by herbivorous insects provides a mechanistic base for several bottom-up cascades. Such a stoichiometric approach has the potential to improve our understanding of bottom-up cascading effects in terrestrial food webs. We suggest a future direction for research by integration of bottom-up cascades and material transfer among trophic levels.

Keywords

Ecological stoichiometry Grazing food chain Herbivorous insects Indirect interaction Tritrophic levels 

Notes

Acknowledgments

We thank T. Hayashi for valuable comments on this manuscript. This research was supported by the 21st Century COE Program to Kyoto University (A14).

References

  1. Andow DA (1991) Vegetational diversity and arthropod population response. Annu Rev Entomol 36:561–586CrossRefGoogle Scholar
  2. Azzouz H, Cherqui A, Campan EDM, Rahbé Y, Duport G, Jouanin L, Kaiser L, Giordanengo P (2005) Effects of plant protease inhibitors, oryzacystatin I and soybean Bowman-Birk inhibitor, on the aphid Macrosiphum euphorbiae (Homoptera, Aphididae) and its parasitoid Aphelinus abdominalis (Hymenoptera, Aphelinidae). J Insect Physiol 51:75–86CrossRefPubMedGoogle Scholar
  3. Barbosa P, Gross P, Kemper J (1991) Influence of plant allelochemicals on the tobacco hornworm and its parasitoid, Cotesia congregata. Ecology 72:1567–1575Google Scholar
  4. Barbosa P, Segarra AE, Gross P, Caldas A, Ahlstrom K, Carlson RW, Ferguson DC, Grissell EE, Hodges RW, Marsh PM, Poole RW, Schauff ME, Shaw SR, Whitfield JB, Woodley NE (2001) Differential parasitism of macrolepidopteran herbivores on two deciduous tree species. Ecology 82:698–704Google Scholar
  5. Baur ME, Boethel DJ (2003) Effects of Bt-cotton expressing CrylA(c) on the survival and fecundity of two hymenopteran parasitoids (Braconidae, Encyrtidae) in the laboratory. Biol Control 26:325–332CrossRefGoogle Scholar
  6. Bjökman C, Bommarco R, Eklund K, Höglund S (2004) Harvesting disrupts biological control of herbivores in a short-rotation coppice system. Ecol Appl 14:1624–1633Google Scholar
  7. Borer ET, Seabloom EW, Shurin JB, Anderson KE, Blanchette CA, Broitman B, Cooper SD, Halpern BS (2005) What determines the strength of a trophic cascade? Ecology 86:528–537Google Scholar
  8. Bouchard É, Cloutier C, Michaud D (2003) Oryzacystatin I expressed in transgenic potato induces digestive compensation in an insect natural predator via its herbivorous prey feeding on the plant. Mol Ecol 12:2439–2446CrossRefPubMedGoogle Scholar
  9. Brose U (2003) Bottom-up control of carabid beetle communities in early successional wetlands: mediated by vegetation structure or plant diversity? Oecologia 135:407–413PubMedGoogle Scholar
  10. Bultman TL, McNeil MR, Goldson SL (2003) Isolate-dependent impacts of fungal endophytes in a multitrophic interaction. Oikos 102:491–496CrossRefGoogle Scholar
  11. Cebrian J (1999) Patterns in the fate of production in plant communities. Am Nat 154:449–468CrossRefPubMedGoogle Scholar
  12. Cowgill SE, Danks C, Atkinson HJ (2004) Multitrophic interactions involving genetically modified potatoes, nontarget aphids, natural enemies and hyperparasitoids. Mol Ecol 13:639–647CrossRefPubMedGoogle Scholar
  13. Denno RF, Fagan WF (2003) Might nitrogen limitation promote omnivory among carnivorous arthropods. Ecology 84:2522–2531Google Scholar
  14. Down RE, Ford L, Woodhouse SD, Raemaekers RJM, Leitch B, Gatehouse JA, Gatehouse AMR (2000) Snowdrop lectin (GNA) has no acute toxic effects on a beneficial insect predator, the 2-spot ladybird (Adalia bipunctata L.). J Insect Physiol 46:379–391CrossRefPubMedGoogle Scholar
  15. Dyer LA, Coley PD (2002) Tritrophic interactions in tropical versus temperate communities. In: Tscharntke T, Hawkins BA (eds) Multitrophic level interactions. Cambridge University Press, Cambridge, pp 67–88Google Scholar
  16. Dyer LA, Letourneau DK (1999) Relative strengths of top-down and bottom-up forces in a tropical forest community. Oecologia 119:265–274CrossRefGoogle Scholar
  17. Dyer LA, Stireman JO III (2003) Community-wide trophic cascades and other indirect interactions in an agricultural community. Basic Appl Ecol 4:423–432CrossRefGoogle Scholar
  18. Fagan WF, Siemann E, Mitter C, Denno RF, Huberty AF, Woods HA, Elser JJ (2002) Nitrogen in insects: implications for trophic complexity and species diversification. Am Nat 160:784–802CrossRefGoogle Scholar
  19. Fonseca CR, Prado PI, Almeida-Neto M, Kubota U, Lewinsohon TM (2005) Flower-heads, herbivores and their parasitoids: food web structure along a fertility gradient. Ecol Entomol 30:36–46CrossRefGoogle Scholar
  20. Forkner PE, Hunter MD (2000) What goes up must come down? Nutrient addition and predation pressure on oak herbivores. Ecology 81:1588–1600Google Scholar
  21. Francis F, Lognay G, Wathelet J, Haubruge E (2001) Effects of allelochemicals from first (Brassicaceae) and second (Myzus persicae and Brevicoryne brassicae) trophic levels on Adalia bipunctata. J Chem Ecol 27:243–256CrossRefPubMedGoogle Scholar
  22. Frost PC, Elser JJ (2002) Growth responses of littoral mayflies to the phosphorus content of their food. Ecol Lett 5:232–240CrossRefGoogle Scholar
  23. Fuentes-Contreras E, Pell JK, Niemeyer HM (1998) Influence of plant resistance at the third trophic level: interactions between parasitoids and entomopathogenic fungi of cereal aphids. Oecologia 117:426–432CrossRefGoogle Scholar
  24. Glendinning JI (2002) How do herbivorous insects cope with noxious secondary plant compounds in their diet? Entomol Exp Appl 104:15–25CrossRefGoogle Scholar
  25. Gratton C, Denno RF (2003) Inter-year carryover effects of a nutrient pulse on Spartina plants, herbivores, and natural enemies. Ecology 84:2692–2707Google Scholar
  26. Groot A, Dicke M (2002) Insect-resistant transgenic plants in a multi-trophic context. Plant J 31:387–406CrossRefPubMedGoogle Scholar
  27. Gross P, Price PW (1988) Plant influences on parasitism of leafminers: a test of enemy free space. Ecology 69:1506–1516Google Scholar
  28. Gruner DS (2004) Attenuation of top-down and bottom-up forces in a complex terrestrial community. Ecology 85:3010–3022Google Scholar
  29. Haddad NM, Haarstad J, Tilman D (2000) The effects of long-term nitrogen loading on grassland insect communities. Oecologia 124:73–84CrossRefGoogle Scholar
  30. Hagen KS (1987) Nutritional ecology of terrestrial insect predator. In: Slansky F, Rodriguez JR (eds) Nutritional ecology of insects, mites, spiders, and related invertebrates. Wiley, New York, pp 533–578Google Scholar
  31. Halaj J, Wise DH (2001) Terrestrial trophic cascades: how much do they trickle? Am Nat 157:262–281CrossRefGoogle Scholar
  32. Hare JD (2002) Plant genetic variation in tritrophic interactions. In: Tscharntke T, Hawkins BA (eds) Multitrophic level interactions. Cambridge University Press, Cambridge, pp 8–43Google Scholar
  33. Harvey JA, Van Dam NM, Gols R (2003) Interactions over four trophic levels: foodplant quality affects development of a hyperparasitoid as mediated through a herbivore and its primary parasitoid. J Anim Ecol 72:520–531CrossRefGoogle Scholar
  34. Havill NP, Raffa KF (2000) Compound effects of induced plant responses on insect herbivores and parasitoids: implications for tritrophic interactions. Ecol Entomol 25:171–179CrossRefGoogle Scholar
  35. Hawes C, Haughton AJ, Osborne JL, Roy DB, Clark SJ, Perry JN, Rothery P, Bohan DA, Brooks DR, Champion GT, Dewar AM, Heard MS, Woiwod IP, Daniels RE, Young MW, Parish AM, Scott RJ, Firbank LG, Squire GR (2003) Responses of plants and invertebrate trophic groups to contrasting herbicide regimes in the farm scale evaluations of genetically modified herbicide-tolerant crops. Phil Trans R Soc Lond B 358:1899–1913CrossRefGoogle Scholar
  36. Holton MK, Lindroth RL, Nordheim EV (2003) Foliar quality influences tree-herbivore–parasitoid interactions: effects of elevated CO2, O3, and plant genotype. Oecologia 137:233–244CrossRefPubMedGoogle Scholar
  37. Hunter MD, Price PW (1992) Playing chutes and ladders: heterogeneity and the relative roles of bottom-up and top-down forces in natural community. Ecology 73:724–732Google Scholar
  38. Kagata H, Nakamura M, Ohgushi T (2005) Bottom-up cascade in a tri-trophic system: different impacts of host-plant regeneration on performance of a willow leaf beetle and its natural enemy. Ecol Entomol 30:58–62CrossRefGoogle Scholar
  39. Karimzadeh J, Bonsall MB, Wright DJ (2004) Bottom-up and top-down effects in a tritrophic system: the population dynamics of Plutella xylostella (L.)–Cotesia plutellae (Kurdjumov) on different host plants. Ecol Entomol 29:285–293CrossRefGoogle Scholar
  40. Karowe DN, Schoonhoven LM (1992) Interactions among three trophic levels: the influence of host plant on performance of Pieris brassicae and its parasitoid, Cotesia glomerata. Entomol Exp Appl 61:241–251CrossRefGoogle Scholar
  41. Knops JMH, Tilman D, Haddad NM, Naeem S, Mitchell CE, Haarstad J, Ritchie ME, Howe KM, Reich PB, Siemann E, Groth J (1999) Effects of plant species richness on invasion dynamics, disease outbreaks, insect abundances and diversity. Ecol Lett 2:286–293CrossRefGoogle Scholar
  42. Koricheva J, Mulder CPH, Schmid B, Huss-Danell JJK (2000) Numerical responses of different trophic groups of invertebrates to manipulations of plant diversity in grasslands. Oecologia 125:271–282CrossRefGoogle Scholar
  43. Langellotto GA, Denno RF (2004) Responses of invertebrate natural enemies to complex-structured habitats: a meta-analytical synthesis. Oecologia 139:1–10CrossRefPubMedGoogle Scholar
  44. Le Rü B, Mitsipa A (2000) Influence of the host plant of the cassava mealybug Phenacoccus manihoti on life-history parameters on the predator Exochomus flaviventris. Entomol Exp Appl 95:209–212CrossRefGoogle Scholar
  45. Lill JT, Marquis RJ (2001) The effects of leaf quality on herbivore performance and attack from natural enemies. Oecologia 126:418–428CrossRefGoogle Scholar
  46. Lindroth RL (1991) Differential toxicity of plant allelochemicals to insects: roles of enzymatic detoxication systems. In: Bernays E (ed) Insect–plant interactions. CRC Press, Boca Raton, pp 1–33Google Scholar
  47. Lövei GL, Arpaia S (2004) The impact of transgenic plants on natural enemies: a critical review of laboratory studies. Entomol Exp Appl 114:1–14CrossRefGoogle Scholar
  48. Martinsen GD, Driebe EM, Whitham TG (1998) Indirect interactions mediated by changing plant chemistry: beaver browsing benefits beetles. Ecology 79:192–200Google Scholar
  49. Masters GJ, Jones TH, Rogers M (2001) Host-plant mediated effects of root herbivory on insect seed predators and their parasitoids. Oecologia 127:246–250CrossRefGoogle Scholar
  50. Matsumura M, Trafelet-Smith GM, Gratton C, Finke DL, Fagan WE, Denno RF (2004) Does intraguild predation enhance predator performance? A stoichiometric perspective. Ecology 85:2601–2615Google Scholar
  51. Mattson WJ (1980) Herbivory in relation to plant nitrogen content. Annu Rev Ecol Syst 11:119–161CrossRefGoogle Scholar
  52. Mayntz D, Toft S (2001) Nutrient composition of the prey’s diet affects growth and survivorship of a generalist predator. Oecologia 127:207–213CrossRefGoogle Scholar
  53. Moe SJ, Stelzer RS, Forman MR, Harpole WS, Daufresne T, Yoshida T (2005) Recent advances in ecological stoichiometry: insights for population and community ecology. Oikos 109:29–39CrossRefGoogle Scholar
  54. Nakamura M, Utsumi S, Miki T, Ohgushi T (2005) Flood initiates bottom-up cascades in a tritrophic system: host plant regrowth increases densities of a leaf beetle and its predators. J Anim Ecol (in press)Google Scholar
  55. Ode PJ, Berenbaum MR, Zangerl AR, Hardy ICW (2004) Host plant, host plant chemistry and the polyembryonic parasitoid Copidosoma sosares: indirect effects in a tritrophic interaction. Oikos 104:388–400CrossRefGoogle Scholar
  56. Pace ML, Cole JJ, Carpenter SR, Kitchell JF (1999) Trophic cascades revealed in diverse ecosystems. Trends Ecol Evol 14:483–488CrossRefPubMedGoogle Scholar
  57. Pasteels JM, Rowell-Rahier M, Raupp MJ (1989) Plant-derived defense in chrysomelid beetles. In: Barbosa P, Letourneau D (eds) Novel aspects of insect–plant interactions. Wiley, New York, pp 235–272Google Scholar
  58. Perkins MC, Woods HA, Harrison JF, Elser JJ (2004) Dietary phosphorus affects the growth of larval Manduca sexta. Arch Insect Biochem Physiol 55:153–168CrossRefPubMedGoogle Scholar
  59. Perner J, Voigt W, Bährmann R, Heinrich W, Marstaller R, Fabian B, Gregor K, Lichter D, Sander FW, Jones TH (2003) Responses of arthropods to plant diversity: changes after pollution cessation. Ecography 26:788–800CrossRefGoogle Scholar
  60. Polis GA (1999) Why are parts of the world green? Multiple factors control productivity and the distribution of biomass. Oikos 86:3–15Google Scholar
  61. Power ME (1992) Top-down and bottom-up forces in food webs: do plants have primacy ? Ecology 73:733–746Google Scholar
  62. Price PW (2002) Resource-driven terrestrial interaction webs. Ecol Res 17:241–247CrossRefGoogle Scholar
  63. Rank NE, Smiley JT (1994) Host-plant effects on Parasyrphus melanderi (Diptera: Syrphidae) feeding on a willow leaf beetle Chrysomela aeneicollis (Coleoptera: Chrysomelidae). Ecol Entomol 19:31–38Google Scholar
  64. Roth S, Knorr C, Lindroth RL (1997) Dietary phenolics affects performance of the gypsy moth (Lepidoptera: Lymantriidae) and its parasitoid Cotesia melanoscela (Hymenoptera: Braconidae). Environ Entomol 26:668–671Google Scholar
  65. Salvo A, Valladares GR (2002) Plant-related intraspecific size variation in parasitoids (Hymenoptera: Parasitica) of a polyphagous leafminer (Diptera: Agromyzidae). Environ Entomol 31:874–879Google Scholar
  66. Schade JD, Kyle M, Hobbie SE, Fagan WF, Elser JJ (2003) Stoichiometric tracking of soil nutrients by a desert insect herbivore. Ecol Lett 6:96–101CrossRefGoogle Scholar
  67. Schmitz OJ, Hambäck PA, Beckerman AP (2000) Trophic cascades in terrestrial systems: a review of the effects of carnivore removals on plants. Am Nat 155:141–153CrossRefPubMedGoogle Scholar
  68. Shurin JB, Borer ET, Seabloom EW, Anderson K, Blanchette CA, Broitman B, Cooper SD, Halpern BS (2002) A cross-ecosystem comparison of the strength of trophic cascades. Ecol Lett 5:758–791CrossRefGoogle Scholar
  69. Siemann E (1998) Experimental tests of effects of plant productivity and diversity on grassland arthropod diversity. Ecology 79:2057–2070Google Scholar
  70. Siemann E, Tilman D, Haarstad J, Ritchie ME (1998) Experimental tests of the dependence of arthropod diversity on plant diversity. Am Nat 152:738–750CrossRefGoogle Scholar
  71. Slansky F, Feeny P (1977) Stabilization of the rate of nitrogen accumulation by larvae of the cabbage butterfly on wild and cultivated food plants. Ecol Monogr 47:209–228Google Scholar
  72. Slansky F, Rodrigues D (eds) (1987) Nutritional ecology of insects, mites, spiders, and related invertebrates. Wiley, New YorkGoogle Scholar
  73. Stamp NE, Yang Y, Osier TL (1997) Responses of an insect predator to prey fed multiple allelochemicals under representative thermal regimes. Ecology 78:203–214Google Scholar
  74. Sterner RW, Elser JJ (2002) Ecological stoichiometry. Princeton University Press, PrincetonGoogle Scholar
  75. Stregbom J, Witzell J, Nordin A, Ericson L (2005) Do multitrophic interactions override N fertilization effects on Operophtera larvae? Oecologia 143:241–250CrossRefPubMedGoogle Scholar
  76. Strong DR (1992) Are trophic cascades all wet? Differentiation and donor-control in speciose ecosystems. Ecology 73:747–754Google Scholar
  77. Sznajder B, Harvey JA (2003) Second and third trophic level effects of differences in plant species reflect dietary specialisation of herbivores and their endoparasitoids. Entomol Exp Appl 109:73–82CrossRefGoogle Scholar
  78. Tabashnik BE, Slansky F (1987) Nutritional ecology of forb foliage-chewing insects. In: Slansky F, Rodrigues JG (eds) Nutritional ecology of insects, mites, spiders, and related invertebrates. Wiley, New York, pp 71–104Google Scholar
  79. Teder T, Tammaru T (2002) Cascading effects of variation in plant vigour on the relative performance of insect herbivores and their parasitoids. Ecol Entomol 27:94–104CrossRefGoogle Scholar
  80. Traugott MS, Stamp NE (1997) Effects of chlorogenic acid- and tomatine-fed caterpillars on performance of an insect predator. Oecologia 109:265–272CrossRefGoogle Scholar
  81. Turlings TC, Gouinguené S, Degen T, Fritzche-Hoballah ME (2002) The chemical ecology of plant–caterpillar–parasitoid interactions. In: Tscharntke T, Hawkins BA (eds) Multitrophic level interactions. Cambridge University Press, Cambridge, pp 148–173Google Scholar
  82. Vitousek P (2004) Nutrient cycling and limitation. Princeton University Press, PrincetonGoogle Scholar
  83. Walde SJ (1995) How quality of host plant affects a predator–prey interaction in biological control. Ecology 76:1206–1219Google Scholar
  84. Walker M, Jones TH (2000) Relative roles of top-down and bottom-up forces in terrestrial tritrophic plant–insect herbivore–natural enemy systems. Oikos 93:177–187CrossRefGoogle Scholar
  85. White TCR (1993) The inadequate environment. Springer, Berlin Heidelberg New YorkGoogle Scholar
  86. Woods HA, Perkins MC, Elser JJ, Harrison JF (2002) Absorption and storage of phosphorus by larval Manduca sexta. J Insect Physiol 48:555–564CrossRefPubMedGoogle Scholar
  87. Zvereva EL, Rank NE (2003) Host plant effects on parasitoid attack on the leaf beetle Chrysomela lapponica. Oecologia 135:258–267PubMedGoogle Scholar

Copyright information

© The Ecological Society of Japan 2005

Authors and Affiliations

  1. 1.Center for Ecological ResearchKyoto UniversityOtsuJapan

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