Oecologia

, Volume 142, Issue 1, pp 90–97

Testing the enemies hypothesis in forest stands: the important role of tree species composition

  • Janne Riihimäki
  • Pekka Kaitaniemi
  • Julia Koricheva
  • Harri Vehviläinen
Community Ecology

Abstract

Numerous studies conducted in agro-ecosystems support the enemies hypothesis, which states that predators and parasites are more efficient in controlling pest densities in polycultures than in monocultures. Few similar studies, however, have been conducted in forest ecosystems, and we do not yet have evidence as to whether the enemies hypothesis holds true in forests. In a 2-year study, we investigated whether the survival of autumnal moth (Epirrita autumnata) larvae and pupae differs between silver birch monocultures and two-species mixtures of birch with black alder, Norway spruce and Scots pine. We placed young larvae on birch saplings and monitored their survival until the end of the larval period, when we checked whether they had been parasitized. After the larvae had pupated, pupal survival was tested in a field trial. In 2002, the larvae disappeared earlier and their overall survival was lower in birch–pine mixtures than in other stand types. In 2003, survival probability was lowest in birch–pine stands only during the first week and there were no differences between stands in overall survival. Larval parasitism was not affected by tree species composition. Pupal weight and pupal survival were likewise not affected by stand type. Among the predators, wood ants were more abundant on birches growing in birch–pine mixtures than in other stand types probably because colonies of myrmecophilic aphids were common on pines. In contrast, spider numbers did not differ between stand types. Ant exclusion by means of a glue ring around the birch trunk increased larval survival, indicating that ants are important predators of the autumnal moth larvae; differences in larval survival between stands are probably due to differential ant predation. Our results provide only partial support for the enemies hypothesis, and suggest that it is both tree species composition and species diversity which affect herbivore survival and predation.

Keywords

Biological control Epirrita autumnata Forest pests Mixed forest Predation 

References

  1. Allison PD (1995) Survival analysis using the SASsystem: a practical guide. SAS Institute, CaryGoogle Scholar
  2. Anderson DR, Burnham KP, Thompson WL (2000) Null hypothesis testing: Problems, prevalence, and an alternative. J Wildl Manage 64:912–923Google Scholar
  3. Andow DA (1991) Vegetational diversity and arthropod population response. Annu Rev Entomol 36:561–586CrossRefGoogle Scholar
  4. Bylund H (1995) Long-term interactions between the autumnal moth and mountain birch: the roles of resources, competitors, natural enemies and weather. PhD thesis, Swedish University of Agricultural SciencesGoogle Scholar
  5. Cappuccino N, Lavertu D, Bergeron Y, Règnière J (1998) Spruce budworm impact, abundance and parasitism rate in a patchy landscape. Oecologia 114:236–242CrossRefGoogle Scholar
  6. Casas J, Aluja M (1997) The geometry of search movements of insects in plant canopies. Behav Ecol 8:37–45Google Scholar
  7. Coll M, Bottrell DG (1994) Effects of nonhost plants on an insect herbivore in diverse habitats. Ecology 75:723–731Google Scholar
  8. Cox DR (1972) Regression models and life tables. J R Stat Soc B 34:187–220Google Scholar
  9. Elton CS (1958) The ecology of invasions by animals and plants. Methuen, LondonGoogle Scholar
  10. Faeth SH, Hammon KE (1997) Fungal endophytes in oak trees: long-term patterns of abundance and associations with leafminers. Ecology 78:810–819Google Scholar
  11. Frank JH (1967) The insect predators of the pupal stage of the winter moth, Operophtera brumata (L.) (Lepidoptera: Hydriomenidae). J Anim Ecol 36:375–389Google Scholar
  12. Gingras D, Dutilleul P, Boivin G (2002) Modeling the impact of plant structure on host-finding behavior of parasitoids. Oecologia 130:396–402CrossRefGoogle Scholar
  13. Haukioja E, Neuvonen S, Hanhimäki S, Niemelä P (1988) The autumnal moth in Fennoscandia. In: Berryman AA (ed) Dynamics of forest insect populations. Patterns, causes, and implications. Plenum, New York, pp 163–178Google Scholar
  14. Hooper DU, Vitousek PM (1997) The effects of plant composition and diversity on ecosystem processes. Science 277:1302–1305CrossRefGoogle Scholar
  15. Horgan FG, Myers JH, Van Meel R (1999) Cyzenis albicans (Diptera: Tachinidae) does not prevent the outbreak of winter moth (Lepidoptera: Geometridae) in birch stands and blueberry plots on the lower mainland of British Columbia. Environ Entomol 28:96–107Google Scholar
  16. Ito F, Higashi S (1991) An indirect mutualism between oaks and wood ants via aphids. J Anim Ecol 60:463–470Google Scholar
  17. Jactel H, Brockerhoff E, Duelli P (2004) A test of the biodiversity-stability theory: meta-analysis of tree species diversity effects on insect pest infestations, and re-examination of responsible factors. In: Scherer-Lorenzen M, Körner C, Schulze E-D (eds) The functional significance of forest diversity. Springer, Berlin Heidelberg New York (in press)Google Scholar
  18. Kaitaniemi P, Ruohomäki K (2001) Sources of variability in plant resistance against insects: free caterpillars show strongest effects. Oikos 98:461–470Google Scholar
  19. Karhu K (1998) Effects of ant exclusion during outbreaks of a defoliator and a sap-sucker on birch. Ecol Entomol 23:185–194CrossRefGoogle Scholar
  20. Kemp WP, Simmons GA (1978) Influence of stand factors on parasitism of spruce budworm eggs by Trichogramma-Minutum. Environ Entomol 7:685–688Google Scholar
  21. Kemp WP, Simmons GA (1979) Influence of stand factors on survival of early instar spruce budworm (Choristoneura fumiferana). Environ Entomol 8:993–996Google Scholar
  22. Koricheva J, Mulder CPH, Schmid B, Joshi J, Huss-Danell K (2000) Numerical responses of different trophic groups of invertebrates to manipulations of plant diversity in grasslands. Oecologia 125:271–282CrossRefGoogle Scholar
  23. Mahdi T, Whittaker JB (1993) Do birch trees (Betula pendula) grow better if foraged by wood ants. J Anim Ecol 62:101–116Google Scholar
  24. McNett BJ, Rypstra AL (2000) Habitat selection in a large orb-weaving spider: vegetational complexity determines site selection and distribution. Ecol Entomol 25:423–432CrossRefGoogle Scholar
  25. Mikola J, Salonen V, Setälä H (2002) Studying the effects of plant species richness on ecosystem functioning: does the choice of experimental design matter? Oecologia 133:594–598CrossRefGoogle Scholar
  26. Moran VC, Southwood TRE (1982) The guild composition of arthropod communities in trees. J Anim Ecol 51:289–306Google Scholar
  27. Pearce JL, Venier LA, McKee J, Pedlar J, McKenney D (2003) Influence of habitat and microhabitat on carabid (Coleoptera: Carabidae) assemblages in four stand types. Can Entomol 135:337–357Google Scholar
  28. Peterson NA, Nilssen AC (1996) Nonlinear temperature-dependent development of autumnal moth pupae, Epirrita autumnata (Lepidoptera: Geometridae). Environ Entomol 25:147–154Google Scholar
  29. Pimentel D (1961) Species diversity and insect population outbreaks. Annu Entomol Soc Am 54:76–86Google Scholar
  30. Punttila P, Haila Y, Pajunen T, Tukia H (1991) Colonization of clear-cut forests by ants in the southern Finnish taiga—a quantitative survey. Oikos 61:250–262Google Scholar
  31. Punttila P, Haila Y, Niemelä J, Pajunen T (1994) Ant communities in fragments of old-growth taiga and managed surroundings. Ann Zool Fenn 31:131–144Google Scholar
  32. Raymond B, Vanbergen A, Watt A, Hartley SE, Cory JS, Hails RS (2002) Escape from pupal predation as a potential cause of outbreaks of the winter moth, Operophtera brumata. Oikos 98:219–228CrossRefGoogle Scholar
  33. Root RB (1973) Organization of a plant-arthropod association in simple and diverse habitats: the fauna of collards (Brassica oleracea). Ecol Monogr 43:95–124Google Scholar
  34. Rosengren R, Vepsäläinen K, Wuorenrinne H (1979) Distribution, nest densities, and ecological significance of wood ants (the Formica rufa -group) in Finland. O.I.L.B. Bull SROP II 3:181–213Google Scholar
  35. Ruohomäki K, Virtanen T, Kaitaniemi P, Tammaru T (1997) Old mountain birches at high altitudes are prone to outbreaks of Epirrita autumnata (Lepidoptera: Geometridae). Environ Entomol 26:1096–1104Google Scholar
  36. Ruohomäki K, Tanhuanpää M, Ayres MP, Kaitaniemi P, Tammaru T, Haukioja E (2000) Causes of cyclicity of Epirrita autumnata (Lepidoptera: Geometridae): grandiose theory and tedious practice. Popul Ecol 42:211–223Google Scholar
  37. Russell EP (1989) Enemies hypothesis: a review of the effect of vegetational diversity on predatory insects and parasitoids. Environ Entomol 18:590–599Google Scholar
  38. Saalas U (1949) Suomen metsähyönteiset. Werner Söderström oy, HelsinkiGoogle Scholar
  39. Saetre P, Brandtberg PO, Lundkvist H, Bengtsson J (1999) Soil organisms and carbon, nitrogen and phosphorus mineralisation in Norway spruce and mixed Norway spruce—Birch stands. Biol Fertil Soils 28:382–388CrossRefGoogle Scholar
  40. SAS (1999) SAS/STAT user’s guide, Version 8. SAS, CaryGoogle Scholar
  41. Sheehan W (1986) Response by specialist and generalist natural enemies to agroecosystem diversification—a selective review. Environ Entomol 15:456–461Google Scholar
  42. Skinner GJ, Whittaker JB (1981) An experimental investigation of inter-relationships between the wood-ant (Formica rufa) and some tree-canopy herbivores. J Anim Ecol 50:313–326Google Scholar
  43. Speight MR, Wainhouse D (1989) Ecology and management of forest insects. Oxford University Press, OxfordGoogle Scholar
  44. Su Q, MacLean DA, Needham TD (1996) The influence of hardwood content on balsam fir defoliation by spruce budworm. Can J For Res 26:1620–1628Google Scholar
  45. Tammaru T (1998) Determination of adult size in a folivorous moth: constraints at instar level? Ecol Entomol 23:80–89CrossRefGoogle Scholar
  46. Tammaru T, Kaitaniemi P, Ruohomäki K (1995) Oviposition choices of Epirrita autumnata (Lepidoptera: Geometridae) in relation to its eruptive population dynamics. Oikos 74:296–304Google Scholar
  47. Tanhuanpää M, Ruohomäki K, Kaitaniemi P, Klemola T (1999) Different impact of pupal predation on populations of Epirrita autumnata (Lepidoptera: Geometridae) within and outside the outbreak range. J Anim Ecol 68:562–570CrossRefGoogle Scholar
  48. Tanhuanpää M, Ruohomäki K, Uusipaikka E (2001) High larval predation rate in non-outbreaking populations of a geometrid moth. Ecology 82:281–289Google Scholar
  49. Teder T, Tanhuanpää M, Ruohomäki K, Kaitaniemi P, Henriksson J (2000) Temporal and spatial variation of larval parasitism in non-outbreaking populations of a folivorous moth. Oecologia 123:516–524CrossRefGoogle Scholar
  50. Tenow O (1972) The outbreaks of Oporinia autumnata Bkh. and Operophtera spp. (Lep. Geometridae) in the Scandinavian mountain chain and northern Finland 1862–1968. Zool Bidr Uppsala 2:1–107Google Scholar
  51. Wardle DA, Bonner KI, Nicholson KS (1997) Biodiversity and plant litter: experimental evidence which does not support the view that enhanced species richness improves ecosystem function. Oikos 79:247–258Google Scholar

Copyright information

© Springer-Verlag 2004

Authors and Affiliations

  • Janne Riihimäki
    • 1
  • Pekka Kaitaniemi
    • 2
  • Julia Koricheva
    • 1
  • Harri Vehviläinen
    • 1
  1. 1.Section of Ecology, Department of BiologyUniversity of TurkuTurkuFinland
  2. 2.Hyytiälä Forestry Field StationUniversity of HelsinkiKorkeakoskiFinland

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