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Oecologia

, Volume 163, Issue 4, pp 949–960 | Cite as

Effects of sap-feeding insect herbivores on growth and reproduction of woody plants: a meta-analysis of experimental studies

  • Elena L. ZverevaEmail author
  • Vojtěch Lanta
  • Mikhail V. Kozlov
Plant-Animal interactions - Original Paper

Abstract

The majority of generalisations concerning plant responses to herbivory are based on studies of natural or simulated defoliation. However, effects caused by insects feeding on plant sap are likely to differ from the effects of folivory. We assessed the general patterns and sources of variation in the effects of sap feeding on growth, photosynthesis, and reproduction of woody plants through a meta-analysis of 272 effect sizes calculated from 52 papers. Sap-feeders significantly reduced growth (−29%), reproduction (−17%), and photosynthesis (−27%); seedlings suffered more than saplings and mature trees. Deciduous and evergreen woody plants did not differ in their abilities to tolerate damage imposed by sap-feeders. Different plant parts, in particular below- and above-ground organs, responded similarly to damage, indicating that sap-feeders did not change the resource allocation in plants. The strongest effects were caused by mesophyll and phloem feeders, and the weakest by xylem feeders. Generalist sap-feeders reduced plant performance to a greater extent than did specialists. Methodology substantially influenced the outcomes of the primary studies; experiments conducted in greenhouses yielded stronger negative effects than field experiments; shorter (<12 months) experiments showed bigger growth reduction in response to sap feeding than longer experiments; natural levels of herbivory caused weaker effects than infestation of experimental plants by sap-feeders. Studies conducted at higher temperatures yielded stronger detrimental effects of sap-feeders on their hosts. We conclude that sap-feeders impose a more severe overall negative impact on plant performance than do defoliators, mostly due to the lower abilities of woody plants to compensate for sap-feeders’ damage in terms of both growth and photosynthesis.

Keywords

Compensatory responses Photosynthesis Plant growth Reproduction Resource allocation 

Notes

Acknowledgments

We are grateful to S. Neuvonen for providing additional information, to A. Stekolshchikov for assistance in search of publications and for consultations on aphid nomenclature, and to anonymous reviewers for valuable suggestions. The study was supported by the Academy of Finland (project number 122133).

Supplementary material

442_2010_1633_MOESM1_ESM.doc (159 kb)
Supplementary material (DOC 159 kb)

References

  1. Atkinson MD (1992) Betula pendula Roth. (B. verrucosa Ehrh.) and B. pubescens Ehrh. J Ecol 80:837–870CrossRefGoogle Scholar
  2. Bale JS, Masters GJ, Hodkinson ID, Awmack C, Bezemer TM, Brown VK, Butterfield J, Buse A, Coulson JC, Farrar J, Good JEG, Harrington R, Hartley S, Jones TH, Lindroth RL, Press MC, Symrnioudis I, Watt AD, Whittaker JB (2002) Herbivory in global climate change research: direct effects of rising temperature on insect herbivores. Glob Chang Biol 8:1–16CrossRefGoogle Scholar
  3. Barbosa P, Schultz JC (1987) Insect outbreaks. Academic, LondonGoogle Scholar
  4. Basset Y (1999) Diversity and abundance of insect herbivores foraging on seedlings in a rainforest in Guyana. Ecol Entomol 24:245–259CrossRefGoogle Scholar
  5. Bernays EA (1998) Evolution of feeding behavior in insect herbivores—success seen as different ways to eat without being eaten. Bioscience 48:35–44CrossRefGoogle Scholar
  6. Bigger DS, Marvier MA (1998) How different would a world without herbivory be? A search for generality in ecology. Integr Biol Issues News Rev 1:60–67CrossRefGoogle Scholar
  7. Boege K, Marquis RJ (2005) Facing herbivory as you grow up: the ontogeny of resistance in plants. Trends Ecol Evol 20:441–448CrossRefPubMedGoogle Scholar
  8. Brodbeck BV, Andersen PC, Mizell RF (1999) Effects of total dietary nitrogen and nitrogen form on the development of xylophagous leafhoppers. Arch Insect Biochem 42:37–50CrossRefGoogle Scholar
  9. Cabrera HM, Argandona VH, Corcuera LJ (1994) Metabolic changes in barley seedlings at different aphid infestation levels. Phytochemistry 35:317–319CrossRefGoogle Scholar
  10. Candolfi MP, Jermini M, Carrera E, Candolfi-Vasconcelos MC (1993) Grapevine leaf gas exchange, plant growth, yield, fruit quality and carbohydrate reserves influenced by the grape leafhopper, Empoasca vitis. Entomol Exp Appl 69:289–296CrossRefGoogle Scholar
  11. Cebrian J, Lartigue J (2004) Patterns of herbivory and decomposition in aquatic and terrestrial ecosystems. Ecol Monogr 74:237–259CrossRefGoogle Scholar
  12. Chapin FS, Schulze ED, Mooney HA (1990) The ecology and economics of storage in plants. Annu Rev Ecol Syst 21:423–447CrossRefGoogle Scholar
  13. Collins CM, Rosado RG, Leather SR (2001) The impact of the aphids Tuberolachnus salignus and Pterocomma salicis on willow trees. Ann Appl Biol 138:133–140CrossRefGoogle Scholar
  14. Crawley MJ (1989) Insect herbivores and plant population dynamics. Annu Rev Entomol 34:531–564CrossRefGoogle Scholar
  15. DeBoo RF, Lowe JH, Dimond JB (1964) Impact of pine leaf aphid Pineus pinifoliae (Chermidae) on its secondary host Eastern white pine. Can Entomol 96:765–772CrossRefGoogle Scholar
  16. Domisch T, Finér L, Neuvonen S, Niemelä P, Risch AC, Kilpeläinen J, Ohashi M, Jurgensen MF (2009) Foraging activity and dietary spectrum of wood ants (Formica rufa group) and their role in nutrient fluxes in boreal forests. Ecol Entomol 34:369–377CrossRefGoogle Scholar
  17. Dungan RJ, Turnbull MH, Kelly D (2007) The carbon costs for host trees of a phloem-feeding herbivore. J Ecol 95:603–613CrossRefGoogle Scholar
  18. Eyles A, Pinkard EA, Mohammed C (2009) Shifts in biomass and resource allocation patterns following defoliation in Eucalyptus globulus growing with varying water and nutrient supplies. Tree Physiol 29:753–764CrossRefPubMedGoogle Scholar
  19. FAO (2006) New_LocClim, Local climate estimator. Version 1.10. Environment and Natural Resources Service—Agrometeorology Group, FAO/SDRN, Rome, ItalyGoogle Scholar
  20. Flynn DFB, Sudderth EA, Bazzaz FA (2006) Effects of aphid herbivory on biomass and leaf-level physiology of Solanum dulcamara under elevated temperature and CO2. Environ Exp Bot 56:10–18CrossRefGoogle Scholar
  21. Furuno T, Nakai I (1987) Effects of the infestation with Pineus harukawai Inouye upon the growth of himekomatsu (Pinus pentaphylla Mayr). Bull Kyoto Univ For 63:1–10Google Scholar
  22. Gurevitch J, Hedges LV (2001) Meta-analysis: combining the results of independent experiments. In: Scheiner SM, Gurevitch J (eds) Design and analysis of ecological experiments. Oxford University Press, New York, pp 347–369Google Scholar
  23. Hawkes CV, Sullivan JJ (2001) The impact of herbivory on plants in different resource conditions: a meta-analysis. Ecology 82:2045–2058CrossRefGoogle Scholar
  24. Herms DA, Mattson WJ (1992) The dilemma of plants—to grow or defend. Q Rev Biol 67:283–335CrossRefGoogle Scholar
  25. Hester AJ, Millard P, Baillie GJ, Wendler R (2004) How does timing of browsing affect above and belowground growth of Betula pendula, Pinus sylvestris and Sorbus aucuparia? Oikos 105:536–550CrossRefGoogle Scholar
  26. Ho LC (1988) Metabolism and compartmentation of imported sugars in sink organs in relation to sink strength. Annu Rev Plant Physiol 39:355–378CrossRefGoogle Scholar
  27. Hódar JA, Zamora R, Castro J, Gómez JM, García D (2008) Biomass allocation and growth responses of Scots pine saplings to simulated herbivory depend on plant age and light availability. Plant Ecol 197:229–238CrossRefGoogle Scholar
  28. Hodkinson ID, Hughes MK (1982) Insect herbivory. Chapman and Hall, LondonGoogle Scholar
  29. Howe GA, Jander G (2008) Plant immunity to insect herbivores. Annu Rev Plant Biol 59:41–66CrossRefPubMedGoogle Scholar
  30. Johnson MTJ, Smith SD, Hausher MD (2009) Plant sex and the evolution of plant defenses against herbivores. Proc Natl Acad Sci USA 106:18079–18084CrossRefPubMedGoogle Scholar
  31. Kaakeh W, Pfeiffer DG, Marini RP (1992) Combined effects of Spirea aphid (Homoptera, Aphididae) and nitrogen fertilization on net photosynthesis, total chlorophyll content, and greenness of apple leaves. J Econ Entomol 85:939–946Google Scholar
  32. Karban R (1980) Periodical cicada nymphs impose periodical oak tree wood accumulation. Nature 287:326–327CrossRefGoogle Scholar
  33. Kozlov MV, Zvereva EL, Zverev VE (2009) Impacts of point polluters on terrestrial biota: comparative analysis of 18 contaminated areas. Springer, DordrechtCrossRefGoogle Scholar
  34. Larson KC (1998) The impact of two gall-forming arthropods on the photosynthetic rates of their hosts. Oecologia 115:161–166CrossRefGoogle Scholar
  35. Larson KC, Whitham TG (1991) Manipulation of food resources by a gall-forming aphid—the physiology of sink-source interactions. Oecologia 88:15–21CrossRefGoogle Scholar
  36. Larson KC, Whitham TG (1997) Competition between gall aphids and natural plant sinks: plant architecture affects resistance to galling. Oecologia 109:575–582CrossRefGoogle Scholar
  37. Llewellyn M (1972) Effects of Lime aphid Eucallipterus tiliae (Aphididae) on growth of lime Tilia × vulgaris Hayne. 1. Energy requirements of aphid population. J Ecol Appl 9:261–282CrossRefGoogle Scholar
  38. Loehle C (1988) Tree life-history strategies—the role of defenses. Can J For Res 18:209–222Google Scholar
  39. Mabry CM, Wayne PW (1997) Defoliation of the annual herb Abutilon theophrasti: mechanisms underlying reproductive compensation. Oecologia 111:225–232CrossRefGoogle Scholar
  40. Macedo TB, Peterson RKD, Weaver DK, Ni XZ (2009) Impact of Diuraphis noxia and Rhopalosiphum padi (Hemiptera: Aphididae) on primary physiology of four near-isogenic wheat lines. J Econ Entomol 102:412–421CrossRefPubMedGoogle Scholar
  41. Marquis RJ (2004) Herbivores rule. Science 305:619–621CrossRefPubMedGoogle Scholar
  42. Mayhead GJ, Jenkins TAR (1992) Growth of young Sitka spruce (Picea sitchensis (Bong.) Carr.) and the effect of simulated browsing, staking and tree shelters. Forestry 65:453–462CrossRefGoogle Scholar
  43. Meyer GA, Whitlow TH (1992) Effects of leaf and sap feeding insects on photosynthetic rates of goldenrod. Oecologia 92:480–489CrossRefGoogle Scholar
  44. Møller AP, Jennions MD (2001) Testing and adjusting for publication bias. Trends Ecol Evol 16:580–586CrossRefGoogle Scholar
  45. Nabity PD, Zavala JA, DeLucia EH (2009) Indirect suppression of photosynthesis on individual leaves by arthropod herbivory. Ann Bot 103:655–663CrossRefPubMedGoogle Scholar
  46. Nagaraj N, Reese JC, Kirkham MB, Kofoid K, Campbell LR, Loughin TM (2002) Relationship between chlorophyll loss and photosynthetic rate in greenbug (Homoptera: Aphididae) damaged Sorghum. J Kans Entomol Soc 75:101–109Google Scholar
  47. Neuvonen S, Routio I, Haukioja E (1992) Combined effects of simulated acid rain and aphid infestation on the growth of Scots pine (Pinus sylvestris) seedlings. Ann Bot Fenn 29:101–106Google Scholar
  48. Nykänen H, Koricheva J (2004) Damage-induced changes in woody plants and their effects on insect herbivore performance: a meta-analysis. Oikos 104:247–268CrossRefGoogle Scholar
  49. O’Connor MI (2009) Warming strengthens an herbivore-plant interaction. Ecology 90:388–398CrossRefPubMedGoogle Scholar
  50. Parker JD, Burkepile DE, Hay ME (2006) Opposing effects of native and exotic herbivores on plant invasions. Science 311:1459–1461CrossRefPubMedGoogle Scholar
  51. Parry WH (1974) Damage caused by green spruce aphid to Norway and Sitka spruce needles. Ann Appl Biol 77:113–120CrossRefGoogle Scholar
  52. Persson IL, Bergstrom R, Danell K (2007) Browse biomass production and regrowth capacity after biomass loss in deciduous and coniferous trees: responses to moose browsing along a productivity gradient. Oikos 116:1639–1650CrossRefGoogle Scholar
  53. Post E, Pedersen C (2008) Opposing plant community responses to warming with and without herbivores. Proc Natl Acad Sci USA 105:12353–12358CrossRefPubMedGoogle Scholar
  54. Puettmann KJ, Saunders MR (2001) Patterns of growth compensation in Eastern white pine (Pinus strobus L.): the influence of herbivory intensity and competitive environments. Oecologia 129:376–384Google Scholar
  55. Rabbinge R, Drees EM, Van der Graaf M, Verberne FCM, Wesselo A (1981) Damage effects of cereal aphids in wheat. Neth J Plant Pathol 87:217–232CrossRefGoogle Scholar
  56. Raven JA (1983) Phytophages of xylem and phloem—a comparison of animal and plant sap-feeders. Adv Ecol Res 13:135–234CrossRefGoogle Scholar
  57. Retuerto R, Fernandez-Lema B, Rodriguez R, Obeso JR (2004) Increased photosynthetic performance in holly trees infested by scale insects. Funct Ecol 18:664–669CrossRefGoogle Scholar
  58. Richards JH (1984) Root growth response to defoliation in two Agropyron bunchgrasses—field observations with an improved root periscope. Oecologia 64:21–25CrossRefGoogle Scholar
  59. Rinnan R, Stark S, Tolvanen A (2009) Responses of vegetation and soil microbial communities to warming and simulated herbivory in a subarctic heath. J Ecol 97:788–800CrossRefGoogle Scholar
  60. Root RB (1973) Organization of a plant-arthropod association in simple and diverse habitats—fauna of collards (Brassica oleracea). Ecol Monogr 43:95–120CrossRefGoogle Scholar
  61. Rosenberg MS (2005) The file-drawer problem revisited: a general weighted method for calculating fail-safe numbers in meta-analysis. Evolution 59:464–468PubMedGoogle Scholar
  62. Rosenberg MS, Adams DC, Gurevitch J (2000) MetaWin: statistical software for meta-analysis. Version 2.0. Sinauer, SunderlandGoogle Scholar
  63. Rosenthal R (1991) Meta-analytic procedures for social research. Sage, Newbury ParkGoogle Scholar
  64. Rummel DR, Quisenberry JE (1979) Influence of thrips (Thysanoptera, Thripidae) injury on leaf development and yield of various cotton genotypes. J Econ Entomol 72:706–709Google Scholar
  65. SAS Institute (2009) SAS version 9.2 for Windows. SAS Institute, CaryGoogle Scholar
  66. Schaffer B, Mason LJ (1990) Effects of scale insect herbivory and shading on net gas exchange and growth of a subtropical tree species (Guaiacum sanctum L.). Oecologia 84:468–473Google Scholar
  67. Schowalter TD (2006) Insect ecology: an ecosystem approach, 2nd edn. Academic, LondonGoogle Scholar
  68. Schowalter TD, Webb JW, Crossley DA (1981) Community structure and nutrient content of canopy arthropods in clear-cut and uncut forest ecosystems. Ecology 62:1010–1019CrossRefGoogle Scholar
  69. Siemann E, Weisser WW (2004) Testing the role of insects in ecosystem functioning. In: Weisser WW, Siemann E (eds) Insects and ecosystem function. Springer, Berlin, pp 383–401CrossRefGoogle Scholar
  70. Smith JP, Schowalter TD (2001) Aphid-induced reduction of shoot and root growth in Douglas fir seedlings. Ecol Entomol 26:411–416CrossRefGoogle Scholar
  71. Stevens MT, Kruger EL, Lindroth RL (2008) Variation in tolerance to herbivory is mediated by differences in biomass allocation in aspen. Funct Ecol 22:40–47Google Scholar
  72. Stiling P, Cornelissen T (2005) What makes a successful biocontrol agent? A meta-analysis of biological control agent performance. Biol Control 34:236–246CrossRefGoogle Scholar
  73. Strauss SY, Agrawal AA (1999) The ecology and evolution of plant tolerance to herbivory. Trends Ecol Evol 14:179–185CrossRefPubMedGoogle Scholar
  74. Tedders WL, Smith JS (1976) Shading effect on pecan by sooty mold growth. J Econ Entomol 69:551–553Google Scholar
  75. Terra WR (1990) Evolution of digestive systems of insects. Annu Rev Entomol 35:181–200CrossRefGoogle Scholar
  76. Trumble JT, Kolodnyhirsch DM, Ting IP (1993) Plant compensation for arthropod herbivory. Annu Rev Entomol 38:93–119CrossRefGoogle Scholar
  77. Varn M, Pfeiffer DG (1989) Effect of rosy apple aphid and Spirea aphid (Homoptera, Aphididae) on dry matter accumulation and carbohydrate concentration in young apple trees. J Econ Entomol 82:565–569Google Scholar
  78. Vranjic JA, Gullan PJ (1990) The effect of a sap-sucking herbivore, Eriococcus coriaceus (Homoptera, Eriococcidae), on seedling growth and architecture in Eucalyptus blakelyi. Oikos 59:157–162CrossRefGoogle Scholar
  79. Welter SC (1989) Arthropod impact on plant gas exchange. In: Bernays EA (ed) Plant–insect interactions. CRC, Boca Raton, pp 135–150Google Scholar
  80. Wolf A, Kozlov MV, Callaghan TV (2008) Impact of non-outbreak insect damage on vegetation in northern Europe will be greater than expected during a changing climate. Clim Chang 87:91–106CrossRefGoogle Scholar
  81. Wood BW, Tedders WL, Thompson JM (1985) Feeding influence of three pecan aphid species on carbon exchange and phloem integrity of seedling pecan foliage. J Am Soc Hortic Sci 110:393–397Google Scholar
  82. Zvereva EL, Kozlov MV (2006) Consequences of simultaneous elevation of carbon dioxide and temperature for plant-herbivore interactions: a meta-analysis. Glob Chang Biol 12:27–41CrossRefGoogle Scholar
  83. Zwolinski JB (1990) Preliminary evaluation of the impact of the pine woolly aphid on condition and growth of pines in the Southern Cape. S Afr For J 153:22–26Google Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • Elena L. Zvereva
    • 1
    Email author
  • Vojtěch Lanta
    • 1
  • Mikhail V. Kozlov
    • 1
  1. 1.Section of Ecology, Department of BiologyUniversity of TurkuTurkuFinland

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