Skip to main content

Advertisement

SpringerLink
Log in

Secondary succession is influenced by belowground insect herbivory on a productive site

  • Plant Animal Interactions
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

We investigated the effects of insect herbivory on a plant community of a productive old-field community by applying foliar and soil insecticides in a full factorial design. During the first 3 years of succession, insecticide treatments had only minor effects on total cover abundance and species richness. However, species ranking within the plant community was strongly affected by soil insecticide but not by foliar insecticide. Creeping thistle, Cirsium arvense , dominated the experimental plots with reduced root herbivory, while square-stemmed willow-herb, Epilobium adnatum , dominated the control and the plots with foliar insecticide. When soil insecticide was applied, cover abundance of monocarpic forbs increased and cover abundance of polycarpic herbs decreased compared to the control. However, this effect was due to a few abundant plant species and is not based on a consistent difference between life history groups. Instead, application of soil insecticide promoted persistence of species that established at the start of succession, and suppressed species that established in the following years. We conclude that below-ground herbivory reduces competitive ability of resident species and, thus, facilitates colonization by late-successional species. Hence, soil insects can exert strong top-down effects on the vegetation of productive sites by affecting dominant plant species and altering competitive balances.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Anonymous (1985) Dursban insecticide: technical information manual. Dow Chemical, Midland, Mich.

    Google Scholar 

  • Bach CE (1994) Effects of a specialist herbivore ( Altica suplicata) on Salix cordata and sand dune succession. Ecol Monogr 64:423–455

    Google Scholar 

  • Barrett GW (1968) The effects of an acute insecticide stress on a semi-enclosed grassland ecosystem. Ecology 6:1019–1035

    Google Scholar 

  • Barrett GW, Darnell RM (1967) Effects of dimethoate on small mammals populations. Am Midl Nat 77:164–175

    Google Scholar 

  • Bentley S, Whittaker JB (1979) Effects of grazing by a chrysomelid beetle, Gastrophysa viridula , on competition between Rumex obtusifolius and Rumex crispus. J Ecol 67:79–90

    Google Scholar 

  • Brown VK (1982) The phytophagous insect community and its impact on early successional habitats. Proceedings of the 5th International Symposium on Insect-Plant Relationship, Wageningen, pp 205–213

  • Brown VK (1990) Insect herbivores, herbivory and plant succession. In: Gilbert F (ed) Insect life cycles. Springer, Berlin Heidelberg New York, pp 183–196

  • Brown VK, Gange AC (1989a) Differential effects of above- and below-ground insect herbivory during early plant succession. Oikos 54:67–76

    Google Scholar 

  • Brown VK, Gange AC (1989b) Herbivory by soil-dwelling insects depresses plant species richness. Funct Ecol 3:667–671

    Google Scholar 

  • Brown VK, Gange AC (1992) Secondary plant succession: how is it modified by insect herbivory? Vegetatio 101:3–13

    Google Scholar 

  • Brown VK, Gange AC (1999) Plant diversity in successional grasslands: how is it modified by foliar insect herbivory? In: Kratochwil A (ed) Biodiversity in ecosystems. Kluwer, Dordrecht, pp 133–146

  • Brown VK, Leijn M, Stinson CA (1987) The experimental manipulation of insect herbivore load by the use of an insecticide (malathion): the effect of application on plant growth. Oecologia 72:77–381

    Google Scholar 

  • Brown VK, Jepson M, Gibson CWD (1988) Insect herbivory: effects on early old-field succession demonstrated by chemical exclusion methods. Oikos 52:293–302

    Google Scholar 

  • Burnham KP, Anderson, DR (1998) Model selection and inference: a practical information-theoretic approach. Springer, Berlin Heidelberg New York

    Google Scholar 

  • Carson WP, Root RB (1999) Top-down effects of insect herbivores during early succession: influence on biomass and plant dominance. Oecologia 121:260–272

    Article  Google Scholar 

  • Carson WP, Root RB (2000) Herbivory and plant species coexistence: Community regulation by an outbreaking phytophagous insect. Ecol Monogr 70:73–99

    Google Scholar 

  • Clay K, Marks S, Cheplick GP (1993) Effects of insect herbivory and fungal endophyte infection on competitive interactions among grasses. Ecology 74:1767–1777

    Google Scholar 

  • Clements RO, Bentley BR, Jackson CA (1986) The impact of granular formulations of phorate, terbufos, carbofuran, carbosulfan and thiofanox on newly sown Italian ryegrass ( Lolium multiflorum). Crop Prot 5:389–394

    CAS  Google Scholar 

  • Crawley MJ (1989) The relative importance of vertebrate and invertebrate herbivores in plant population dynamics. In: Bernays B (ed) Insect-plant interactions. CRC, Boca Raton, pp 45–71

  • Crawley MJ (1997) Plant-herbivore dynamics. In: Crawley MJ (ed) Plant ecology. Blackwell, Oxford, pp 401–474

  • Crutchfield BA, Potter DA (1995) Tolerance of cool-season turfgrass to feeding by Japanese beetle and southern masked chafer (Coleoptera: Scarabaeidae) grubs. J Econ Entomol 88:1380–1387

    Google Scholar 

  • Davidson DW (1993) The effects of herbivory and granivory on terrestrial plant succession. Oikos 68:25–35

    Google Scholar 

  • Dell’Omo G, Shore RF (1996) Behavioral effects of acute sublethal exposure to dimethoate on wood mice, Apodemus sylvaticus. II. Field studies on radio tagged mice in a cereal ecosystem. Arch Environ Contamin Toxicol 31:538–542

    CAS  Google Scholar 

  • Domsch KH (1992) Pestizide im Boden—Mikrobieller Abbau und Nebenwirkungen auf Mikroorganismen. VCH, Weinheim

  • Eber S, Brandl R (2003) Regional patch dynamics of the weed Cirisum arvense, and possible implications for plant-animal interactions. J Veg Sci 14:259–266

    Google Scholar 

  • Edwards PJ, Bourdot GW, Crawley MJ (2000) Influence of herbivory, competition and soil fertility on the abundance of Cirsium arvense in acid grassland. J Appl Ecol 37:321–334

    Article  Google Scholar 

  • Foster BL, Gross KL (1998) Species richness in a successional grassland: effects of nitrogen enrichment and plant litter. Ecology 79:2593–2602

    Google Scholar 

  • Frampton GK (1999) Spatial variation in non-target effects of the insecticides chlorpyrifos, cypermethrin and pirimicarb on Collembola in winter wheat. Pestic Sci 55:875–886

    CAS  Google Scholar 

  • Fraser LH (1998) Top-down versus bottom-up control influenced by productivity in a North Derbyshire, UK, dale. Oikos 81:99–108

    Google Scholar 

  • Fraser LH, Grime JP (1997) Primary productivity and trophic dynamics investigated in a North Derbyshire, UK, dale. Oikos 80:499–508

    Google Scholar 

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

    Article  Google Scholar 

  • Fretwell SD (1977) The regulation of plant communities by food chains exploiting them. Perspect Biol Med 20:169–185

    Google Scholar 

  • Fretwell SD (1987) Food chain dynamics: the central theory of ecology? Oikos 50:91–301

    Google Scholar 

  • Ganade G, Brown VK (1997) Effects of below-ground insects, mycorrhizal fungi and soil fertility on the establishment of Vicia in grassland communities. Oecologia 109:374–381

    Article  Google Scholar 

  • Gange AC, Brown VK, Farmer LM (1992) Effects of pesticides on the germination of weed seeds: implications for manipulative experiments. J Appl Ecol 29:303–310

    Google Scholar 

  • Gibson CWD, Brown VK, Jepsen M (1987) Relationships between the effects of insect herbivory and sheep grazing on seasonal changes in an early successional plant community. Oecologia 71:245–253

    Google Scholar 

  • Gibson DJ, Freeman CC, Hulbert LC (1990) Effects of small mammal and invertebrate herbivory on plant species richness and abundance in tallgrass prairie. Oecologia 84:169–175

    Google Scholar 

  • Greig-Smith P (1983) Quantitative plant ecology. University of California Press, Berkley

  • Hendrix SD, Brown VK, Gange AC (1988) Effects of insect herbivory on early plant succession: comparison of an English site and an American Site. Biol J Linn Soc 35:205–216

    Google Scholar 

  • Hulme PE (1996) Herbivores and the performance of grassland plants: a comparison of arthropod, mollusc and rodent herbivory. J Ecol 84:43–51

    Google Scholar 

  • Jackson WB (1952) Populations of the white-footed mouse ( Peromyscus leucopus) subjected to the application of DDT and parathion. Ecol Monogr 22:259–281

    Google Scholar 

  • Jagers op Akkerhuis GAJM, Damgaard C, Kjaer C, Elmegaard N (1999) Comparison of the toxicity of dimethoate and cypermethrin in the laboratory and the field when applying the same bioassay. Environ Toxicol Chem 18:2379–2385

    Google Scholar 

  • Jung G, Schädler M, Auge H, Brandl R (2000) Effects of herbivorous insects on secondary plant succession. Mitt Dtsch Ges Allg Angew Entomol 12:169–172

    Google Scholar 

  • Keselman HJ, Algina J, Kowalchuk RK, Wolfinger RD (1999) A comparison of recent approaches to the analysis of repeated measurements. Br J Math Stat Psychol 52:63–78

    Article  Google Scholar 

  • Little RC, Henry PR, Ammerman CB (1998) Statistical analysis of repeated measures data using SAS procedures. J Anim Sci 76:216–1231

    Google Scholar 

  • Louda SM, Keeler V, Holt RD (1990). Herbivore influence on plant performance and competitive interactions. In: Grace JB, Tilman D (eds) Perspectives on plant competition. Academic Press, New York, pp 413–444

  • McBrien H, Harmson R, Crowder A (1983) A case of insect grazing affecting plant succession. Ecology 64:1035–1039

    Google Scholar 

  • Mulder CPH, Koricheva J, HussDanell K, Hogberg P, Joshi J (1999) Insects affect relationships between plant species richness and ecosystem processes. Ecol Lett 2:237–246

    Article  Google Scholar 

  • Newman JA, Bergelson J, Grafen A (1997) Blocking factors and hypothesis tests in ecology: is your statistics text wrong? Ecology 78:1312–1320

    Google Scholar 

  • Oksanen L (1990) Predation, herbivory, and plant strategies along gradients of primary productivity. In: Grace JB, Tilman D (eds) Perspectives on plant competition. Academic Press, San Diego, pp 445–474

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

    PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Pacala SW, Crawley MJ (1992) Herbivores and plant diversity. Am Nat 40:243–260

    Article  Google Scholar 

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

    PubMed  Google Scholar 

  • Potter DA, Patterson CG, Redmond CT (1992) Influence of turfgrass species and tall fescue endophyte on feeding ecology of Japanese beetle and southern masked chafer grubs (Coleoptera: Scarabaeidae). J Econ Entomol 85:900–909

    Google Scholar 

  • Schädler M, Jung G, Auge H, Brandl R (2003a) Does the Fretwell-Oksanen model apply to invertebrates? Oikos 100:203–207

    Google Scholar 

  • Schädler M, Jung G, Auge H, Brandl R (2003b) Palatability, decomposition and insect herbivory: patterns in a successional old-field plant community. Oikos 103:121–132

    Article  Google Scholar 

  • Schmitz OJ (2003) Top predator control of plant biodiversity and productivity in an old-field ecosystem. Ecol Lett 6:156–163

    Article  Google Scholar 

  • Schowalter TD (1981) Insect herbivore relationship to the state of host plant: biotic regulation of ecosystem nutrient cycling through ecological succession. Oikos 37:126–130

    Google Scholar 

  • Sokal RR, Rohlf FJ (1997) Biometry, 3rd edn. Freeman, New York

  • Solomon KR, Giesy JP, Kendall RJ, Best LB, Coats JR, Dixon KR, Hooper MJ, Kenaga EE, McMurry ST (2001) Chlorpyrifos: ecotoxicological risk assessment for birds and mammals in corn agroecosystems. Human Ecol Risk Assess 7:497–632

    CAS  Google Scholar 

  • Spokes JR, MacDonald RM, Hayman DS (1981) Effects of plant protection chemicals on vesicular-arbuscular mycorrhizas. Pestic Sci 12:346–350

    CAS  Google Scholar 

  • Tomlin C (1994) The pesticide manual. British Crop Protection Council, Farnham

  • Uriarte M, Schmitz OJ (1998) Trophic control across a natural productivity gradient with sap-feeding herbivores. Oikos 82:552–560

    Google Scholar 

  • Wardle DA (2002) Communities and ecosystems—linking the above ground and below ground components. Princeton University Press, Princeton

  • Wilby A, Brown VK (2001) Herbivory, litter and soil disturbance as determinants of vegetation dynamics during early old-field succession under set-aside. Oecologia 127:259–265

    Article  Google Scholar 

  • Wilcox A (1998) Early plant succession on former arable land. Agric Ecosyst Environ 69:143–157

    Article  Google Scholar 

  • Witsack W, Al-Hussein IA, Süssmuth T (1995) Analyse der Faunenstrukturveränderung bei der Regeneration hochbelasteter Agrarökosysteme (epigäische Fauna). In: Körschens M, Mahn EG (eds) Strategien zur Regeneration belasteter Agrarökosysteme des mitteldeutschen Schwarzerdegebietes. Teubner, Stuttgart, pp 423–462

  • Xiong SJ, Nilsson C (1999) The effects of plant litter on vegetation: a meta-analysis. J Ecol 87:984–994

    Google Scholar 

Download references

Acknowledgements

We are grateful to Katharina Leib for her assistance in the field, and thank James Cahill and Daniel Prati for valuable comments on earlier drafts of the manuscript.

Author information

Author notes

  1. Martin Schädler

    Present address: Faculty of Biology, Department of Animal Ecology, Philipps-University Marburg, Karl-von-Frisch-Strasse, 35032 , Marburg, Germany

  2. Roland Brandl

    Present address: Faculty of Biology, Department of Animal Ecology, Philipps-University Marburg, Karl-von-Frisch-Strasse, 35032 , Marburg, Germany

Authors and Affiliations

  1. Department of Community Ecology, UFZ Centre for Environmental Research Leipzig-Halle, Theodor-Lieser-Strasse 4, 06120, Halle, Germany

    Martin Schädler, Gertraud Jung, Roland Brandl & Harald Auge

Authors
  1. Martin Schädler
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Gertraud Jung
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Roland Brandl
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Harald Auge
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Martin Schädler.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Schädler, M., Jung, G., Brandl, R. et al. Secondary succession is influenced by belowground insect herbivory on a productive site. Oecologia 138, 242–252 (2004). https://doi.org/10.1007/s00442-003-1425-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-003-1425-y

Keywords

Search

Navigation