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Do multitrophic interactions override N fertilization effects on Operophtera larvae?

  • Plant Animal Interactions
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Abstract

We examined how performance of Operophtera brumata (Lepidoptera) larvae was affected by nitrogen (N) fertilization of boreal forest understorey vegetation. We monitored larval densities on Vaccinium myrtillus plants for a period of 7 years in a field experiment. Preliminary results indicated that the N effect on larval densities was weak. To examine if this was due to indirect interactions with a plant pathogen, Valdensia heterodoxa, that share the same host plant, or due to top-down effects of predation, we performed both a laboratory feeding experiment (individual level) and a bird exclusion experiment (population level) in the field. At the individual level, altered food plant quality (changes in plant concentration of carbon, N, phenolics, or condensed tannins) due to repeated infection by the pathogen had no effect on larval performance, but both survival to the adult stage and adult weight were positively affected by N fertilization. Exclusion of insectivorous birds increased the frequency of larval damage on V. myrtillus shoots, indicating higher larval densities. This effect was stronger in fertilized than in unfertilized plots, indicating higher bird predation in fertilized plots. Predation may thus explain the lack of fertilization effect on larval densities in the field experiment. Our results suggest that top-down effects are more important for larval densities than bottom-up effects, and that bird predation may play an important role in population regulation of O. brumata in boreal forests.

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References

  • Ahti T, Hämet-Ahti L, Jalas J (1968) Vegetation zones and their sections in Northwestern Europe. Ann Bot Fenn 5:169–211

    Google Scholar 

  • Atlegrim O (1989) Exclusion of birds from bilberry stands: impact on insect larval and damage to the bilberry. Oecologia 79:136–139

    Article  Google Scholar 

  • Baylis M, Pierce NE (1991) The effect of host-plant quality on the survival of larvae and oviposition by adults of an ant-tended lyceaid butterfly, Jalmenus evagoras. Ecol Entomol 16:1–9

    Google Scholar 

  • Carpenter SR, Cole J, Hodgson JR, Kitchell JF, Pace ML, Bade D, Cottingham KL, Essington TE, Houser JN, Schindler DE (2001) Trophic cascades, nutrients, and lake productivity: whole-lake experiments. Ecol Monogr 71:163–186

    Google Scholar 

  • Chapin III SF (1980) The mineral nutrition of wild plants. Annu Rev Ecol Syst 11:233–260

    Article  Google Scholar 

  • Dixon RA, Paiva NL (1995) Stress-induced phenylpropanoid metabolism. Plant Cell 7:1085–1097

    Article  CAS  PubMed  Google Scholar 

  • Eriksson B (1974) On Deuteromycetes on Diapensales and Ericales in Fennoscandia. Sven Bot Tidskr 68:235–253

    Google Scholar 

  • Feeny P (1970) Seasonal changes in oak leaf tannins and nutrients as a cause of spring feeding winter moth caterpillars. Ecology 51:565–581

    Google Scholar 

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

    Google Scholar 

  • Fowler SV, Lawton JH (1985) Rapidly induced defenses and talking trees: the devil’s advocate position. Am Nat 126:181–195

    Article  Google Scholar 

  • Fraser LH, Grime JP (1998) Top-down control and its effect on the biomass and composition of three grasses ay high and low soil fertility in outdoor microcosmos. Oecologia 113:239–246

    Article  Google Scholar 

  • Gruner DS (2004) Attenuation of top-down and bottom-up forces in a complex terrestrial community. Ecology 85:3010–3022

    Google Scholar 

  • Häggström H, Larsson S (1995) Slow larval growth on a suboptimal willow results in high predation mortality in the leaf beetle Galerucella lineola. Oecologia 104:308–315

    Article  Google Scholar 

  • Hammond AM, Hardy TN (1988) Quality of diseased plants as hosts for insects. In: Heinrichs EA (ed) Plant stress-insect interactions. Wiley, New York, pp 341–382

    Google Scholar 

  • Hatcher PE (1995) Three-way interactions between plant pathogenic fungi, herbivorous insects and their host plants. Biol Rev 70:639–694

    Google Scholar 

  • Hatcher PE, Paul ND, Ayers PG, Whittaker JB (1995) Interactions between Rumex spp., herbivores and a rust fungus: the effect of Uromyces rumicis infection on leaf nutritional quality. Funct Ecol 9:97–105

    Google Scholar 

  • Holliday RT (1977) Population ecology of winter moth (Operophtera brumata) on apple in relation to larval dispersal and time of bud burst. J Appl Ecol 14:803–813

    Google Scholar 

  • Holmes RT, Schultz JC, Nothnagel P (1979) Bird predation on forest insects: an exclusure experiment. Science 206:462–463

    Google Scholar 

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

    Article  Google Scholar 

  • Hunter MD, Price PW (1998) Cycles in insect populations: delayed density dependence or exogenous driving variables? Ecol Entomol 23:216–222

    Google Scholar 

  • Kause A, Ossipov V, Haukioja E, Lempa K, Hanhimäki S, Ossipova S (1999) Multiplicity of biochemical factors determining quality of growing birch leaves. Oecologia 120:102–112

    Article  Google Scholar 

  • Kerslake JE, Kruuk LEB, Hardey SE, Woodin SJ (1996) Winter moth (Operophtera brumata (Lepidoptera: Geometridae)) outbreaks on Scottis heather moorlands: effects of host plant and parasitoids on larval survival and development. Bull Entomol Res 86:155–164

    Google Scholar 

  • Kytö M, Niemelä P, Larsson S (1996) Insects on trees: population and individual response to fertilization. Oikos 75:148–159

    Google Scholar 

  • Lappalainen J, Helander ML, Palokangas P (1995) The performance of the autumnal moth is lower on trees infected by birch rust. Mycol Res 99:994–996

    Google Scholar 

  • Larsson S (1989) Stressful times for plant stress-insect performance hypothesis. Oikos 56:277–283

    Google Scholar 

  • Leather SR (1988) Size reproductive potential and fecundity in insects: things aren’t as simple as they seem. Oikos 51:386–389

    Google Scholar 

  • Marquis RJ, Whelan CJ (1994) Insectivorous birds increase growth of white oak trough consumption of leaf-chewing insects. Ecology 75:2007–2014

    Google Scholar 

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

    Article  Google Scholar 

  • Moran PJ (1998) Plant-mediated interactions between insects and a fungal plant pathogen and the role of plant chemical response to infection. Oecologia 115:523–530

    Article  Google Scholar 

  • Nordin A, Näsholm T, Ericson L (1998) Effects of simulated N deposition on understorey vegetation of boreal coniferous forest. Funct Ecol 12:691–699

    Article  Google Scholar 

  • Norvell LL, Redhead SA (1994) Valdensinia heterodoxa (Sclerotiniaceae) in the United States. Can J For Res 24:1981–1983

    Google Scholar 

  • Oksanen L, Oksanen T (2000) The logic and realism of the hypothesis of exploitation ecosystems. Am Nat 155:703–723

    Article  Google Scholar 

  • Oksanen L, Fretwell SD, Arrunda J, Niemela P (1981) Exploitation systems in gradients of primary productivity. Am Nat 118:240–262

    Article  Google Scholar 

  • Paine RT (1980) Food webs: linkage, interaction strength, and community infrastructure. J Anim Ecol 49:667–685

    Google Scholar 

  • Parry D, Spence JR, Volney JA (1998) Budbreak phenology and natural enemies mediate survival of first-instar forest tent caterpillar (Lepidoptera:Lasiocampidae). Environ Entomol 27:1368–1374

    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? Mulitipel factors control productivity and the distribution of biomass. Oikos 86:3–15

    Google Scholar 

  • Polis GA, Sears ALW, Huxel GR, Strong DR, Maron J (2000) When is a trophical cascade a trophical cascade? Trends Ecol Evol 15:473–475

    Article  PubMed  Google Scholar 

  • Power ME (1992) Top-down and bottom-up forces in food webs: do plants have primacy? Ecology 74:673–684

    Google Scholar 

  • Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225

    Google Scholar 

  • Ritchie ME (2000) Nitrogen limitation and trophic vs. abiotic influences on insect herbivores in a temperate grassland. Ecology 8:1601–1612

    Google Scholar 

  • Ritchie ME, Tilman D (1993) Predictions of species interactions from consumer-resource theory: experimental test with grasshoppers and plants. Oecologia 94:516–527

    Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Scriber JM, Slansky F Jr (1981) The nutritional ecology of immature insects. Annu Rev Entomol 26:183–211

    Google Scholar 

  • Sipura M (1999) Tritrophic interactions: willows, herbivorous insects and insectivorous birds. Oecologia 121:537–545

    Article  Google Scholar 

  • Solomon PS, Oliver RP (2001) The nitrogen content of tomato leaf apoplast increases during infection by Cladosporium fulvum. Planta 213:241–249

    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 

  • Strengbom J, Nordin A, Näsholm T, Ericson L (2002) Parasitic fungus mediates vegetation change in nitrogen exposed boreal forest. J Ecol 90:61–67

    Article  Google Scholar 

  • Strong DR (1992) Are trophic cascades all wet? The redundant differentiation in trophic architecture of high diversity ecosystems. Ecology 73:747–754

    Google Scholar 

  • Sun B, Ricardo-da-Silva J, Spranger I (1998) Critical factors of vanillin assay for catechins and proanthocyanidins. J Agri Food Chem 46:4267–4274

    Google Scholar 

  • Tamm CO (1991) Nitrogen in terrestrial ecosystems. Ecological studies no 81. Springer, Berlin Heidelberg New York

  • Tikkanen O-P, Julkunen-Tiitto R (2003) Phenological variation as protection against defoliating insects: the case of Quercus robur and Operophtera brumata. Oecologia 136:244–251

    Article  PubMed  Google Scholar 

  • Tikkanen O-P, Carr TG, Roininen H (1999) Factors influencing the distribution of a generalist spring-feeding moth, Operophtera brumata (Lepidoptera: Geometridae) on host plants. Environ Entomol 3:461–469

    Google Scholar 

  • White TCS (1993) The inadequate environment. Nitrogen and the abundance of animals. Springer, Berlin Heidelberg New York

    Google Scholar 

  • Wint W (1983) The role of alternative host-plant species in the life of a polyphagous moth, Operophtera brumata (Lepidoptera: Geometridae). J Anim Ecol 52:439–450

    Google Scholar 

  • Witzell J, Shevtsova A (2004) Nitrogen-induced changes in phenolics of Vaccinium myrtillus—implications for the interaction with a parasitic fungus. J Chem Ecol 30:1919–1938

    Google Scholar 

  • Witzell J, Gref R, Näsholm T (2003) Plant-part specific and temporal variation in phenolic compounds of boreal bilberry (Vaccinium myrtillus L.) plants. Biochem Syst Ecol 31:115–127

    Google Scholar 

  • Zar JH (1996) Biostatistical analysis. Prentice-Hall, New Jersey

    Google Scholar 

Download references

Acknowledgements

We would like to thank The Svartberget Experimental Forest and its personnel for assistance with the annual fertilization of the experimental plots; Prof. Matt Ayres, Dr. Olli-Pekka Tikkanen, and two anonymous reviewer for valuable comments on an earlier version of this paper. This study was financially supported through grants from the ASTA program financially supported by MISTRA (Swedish Foundation for Strategic Environmental Research) (to LE and AN), by the Swedish Research Council (VR) (to LE), by FORMAS (Swedish Research Council for Environment, Agricultural Sciences and Spatial Planning) (to AN and JW), and by the Gunnar & Ruth Björkman fod För Norrländsk Botanisk Forskning (to JS). The work presented in this paper conforms to the legal requirements of the country in which it was carried out, including those relating to conservation and welfare.

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Strengbom, J., Witzell, J., Nordin, A. et al. Do multitrophic interactions override N fertilization effects on Operophtera larvae?. Oecologia 143, 241–250 (2005). https://doi.org/10.1007/s00442-004-1799-5

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