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Oecologia

, Volume 141, Issue 1, pp 47–56 | Cite as

Reduction in size and fecundity of the autumnal moth, Epirrita autumnata, in the increase phase of a population cycle

  • Tero KlemolaEmail author
  • Kai Ruohomäki
  • Tommi Andersson
  • Seppo Neuvonen
Population Ecology

Abstract

Increasing fecundity with increasing density has been observed for many cyclic herbivore populations, including some forest Lepidoptera. We monitored population density, body size and reproductive capacity of the cyclic lepidopteran, the autumnal moth (Epirrita autumnata, Geometridae), from the early increase phase to the devastating outbreak density in northernmost Norway. Larval density of the species increased exponentially from 1998 to 2002 and remained at the outbreak level also in 2003. Within the same period, the body size and fecundity of individuals reduced as analysed from several parallel datasets on larvae, pupae and adults. In another study area in northernmost Finland, the density increase of the autumnal moth was moderate only, and true outbreak density was not attained during the study. Despite that, a reduction was again detected in the size and fecundity of individuals. Possible factors responsible for the reduced size and fecundity of individuals in the Norwegian population were quantitative shortage of foliage, rapid and delayed inducible resistances of the host, mountain birch (Betula pubescens ssp. czerepanovii), as well as crowding-induced responses of larvae. These factors likely acted in concert, although non-delayed responses to the density were emphasized. Our findings did not support the hypotheses of climatic release, inducible susceptibility of the host tree and mast depression (i.e. lowered chemical defence of the host tree after its mast seeding) as promoters of the fecundity-based density increase of the autumnal moth, since the reduced fecundity in relation to increased density was strongly against the predictions of these hypotheses. Therefore, we suggest that the density increase of autumnal moth populations is promoted by high survival rather than exceptionally high fecundity.

Keywords

Chitty effect Forest Lepidoptera Inducible resistance Insect outbreak Mountain birch 

Notes

Acknowledgements

We would like to thank Kevo Subarctic Research Institute for the use of facilities and Fiia Haavisto, Heini Hyvärinen, Piia Juntunen, Pekka Kaitaniemi, Emma Kosonen, Marjukka Kulmala, Sanna Laakso, Elina Mäntylä, Lauri Nikkinen, Mikko Paajanen, Varpu Vahtera and Harri Vehviläinen for their assistance with fieldwork. Sinikka Hanhimäki provided data for the size-fecundity relationships. The manuscript benefited from the comments of Matthew P. Ayres, Erkki Haukioja, Otso Huitu and an anonymous referee. People working for Statskog in Norway are thanked for their sympathetic attitude to Finnish research. This research was financially supported by the Academy of Finland (project 204190 to T. K. and project 48697 to K. R.) and the Emil Aaltonen Foundation (grant to T. K.).

References

  1. Baltensweiler W, Benz G, Bovey P, Delucchi V (1977) Dynamics of larch bud moth populations. Annu Rev Entomol 22:79–100CrossRefGoogle Scholar
  2. Berryman AA (1987) The theory and classification of outbreaks. In: Barbosa P, Schultz JC (eds) Insect outbreaks. Academic, San Diego, Calif., pp 3–29Google Scholar
  3. Berryman AA (1996) What causes population cycles of forest Lepidoptera? Trends Ecol Evol 11:28–32CrossRefGoogle Scholar
  4. Blais JR, Prentice RM, Sippell WL, Wallace DR (1955) Effects of weather on the forest tent caterpillar, Malacosoma disstria Hbn., in central Canada in the spring of 1953. Can Entomol 87:1–8Google Scholar
  5. Boonstra R, Krebs CJ (1979) Viability of large- and small-sized adults in fluctuating vole populations. Ecology 60:567–573Google Scholar
  6. Campbell RW (1978) Some effects of gypsy moth density on rate of development, pupation time, and fecundity. Ann Entomol Soc Am 71:442–448Google Scholar
  7. Chitty D (1952) Mortality among voles (Microtus agrestis) at Lake Vyrnwy, Montgomeryshire in 1936–1939. Philos Trans R Soc Lond Ser B Biol Sci 236:505–552Google Scholar
  8. Chitty D (1967) The natural selection of self-regulatory behaviour in animal populations. Proc Ecol Soc Aust 2:51–78Google Scholar
  9. Chitty D (1996) Do lemmings commit suicide? Beautiful hypotheses and ugly facts. Oxford University Press, New YorkGoogle Scholar
  10. Christian JJ (1950) The adreno-pituitary system and population cycles in mammals. J Mammal 31:247–259Google Scholar
  11. Dicke M, Agrawal AA, Bruin J (2003) Plants talk, but are they deaf? Trends Plant Sci 8:403–405CrossRefPubMedGoogle Scholar
  12. Elton CJ (1924) Periodic fluctuations in the numbers of animals: their causes and effects. Br J Exp Biol 2:119–163Google Scholar
  13. Ergon T, Lambin X, Stenseth NC (2001) Life-history traits of voles in a fluctuating population respond to the immediate environment. Nature 411:1043–1045CrossRefPubMedGoogle Scholar
  14. Greenbank DO (1956) The role of climate and dispersal in the initiation of outbreaks of the spruce budworm in New Brunswick. Can J Zool 34:453–476Google Scholar
  15. Hanhimäki S, Senn J (1992) Sources of variation in rapidly inducible responses to leaf damage in the mountain birch-insect herbivore system. Oecologia 91:318–331Google Scholar
  16. Hansson L (1969) Spring populations of small mammals in central Swedish Lapland in 1964–1968. Oikos 20:431–450Google Scholar
  17. Haukioja E (1982) Inducible defences of white birch to a geometrid defoliator, Epirrita autumnata. In: Visser JH, Minks AK (eds) Proceedings of the 5th International Symposium on Insect-Plant Relationships. Pudoc, Wageningen, pp 199–203Google Scholar
  18. Haukioja E (1990) Induction of defenses in trees. Annu Rev Entomol 36:25–42CrossRefGoogle Scholar
  19. Haukioja E, Hanhimäki S (1985) Rapid wound-induced resistance in white birch (Betula pubescens) foliage to the geometrid Epirrita autumnata: a comparison of trees and moths within and outside the outbreak range of the moth. Oecologia 65:223–228Google Scholar
  20. Haukioja E, Neuvonen S (1985a) The relationship between size and reproductive potential in male and female Epirrita autumnata (Lep., Geometridae). Ecol Entomol 10:267–270Google Scholar
  21. Haukioja E, Neuvonen S (1985b) Induced long-term resistance of birch foliage against defoliators: defensive or incidental? Ecology 66:1303–1308Google Scholar
  22. Haukioja E, Neuvonen S (1987) Insect population dynamics and induction of plant resistance: the testing of hypotheses. In: Barbosa P, Schultz JC (eds) Insect outbreaks. Academic, San Diego, Calif., pp 411–432Google Scholar
  23. 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
  24. Haukioja E, Ruohomäki K, Senn J, Suomela J, Walls M (1990) Consequences of herbivory in the mountain birch (Betula pubescens ssp. tortuosa): importance of the functional organization of the tree. Oecologia 82:238–247Google Scholar
  25. Hogstad O (1996) Morphological changes of Epirrita autumnata Bkh. and Operophtera brumata (L.) (Lep., Geometridae) during a mass outbreak in a subalpine birch forest in Central Norway. Fauna Norv Ser B 43:47–57Google Scholar
  26. Johnson JB, Omland KS (2004) Model selection in ecology and evolution. Trends Ecol Evol 19:101–108CrossRefGoogle Scholar
  27. Kaitaniemi P, Ruohomäki K (2001) Sources of variability in plant resistance against insects: free caterpillars show strongest effects. Oikos 95:461–470Google Scholar
  28. Kaitaniemi P, Ruohomäki K, Haukioja E (1997) Consumption of apical buds as a mechanism of alleviating host plant resistance for Epirrita autumnata larvae. Oikos 78:230–238Google Scholar
  29. Kaitaniemi P, Ruohomäki K, Tammaru T, Haukioja E (1999) Induced resistance of host tree foliage during and after a natural insect outbreak. J Anim Ecol 68:382–389CrossRefGoogle Scholar
  30. Kalela O (1957) Regulation of reproduction rate in subarctic populations of the vole, Clethrionomys rufocanus. Ann Acad Sci Fenn Ser A IV 34:1–60Google Scholar
  31. Kallio P, Lehtonen J (1973) Birch forest damage caused by Oporinia autumnata (Bkh.) in 1965–1966 in Utsjoki, N. Finland. Rep Kevo Subarct Res Stn 10:55–69Google Scholar
  32. Karban R, Baldwin IT (1997) Induced responses to herbivory. University of Chicago Press, Chicago, Ill.Google Scholar
  33. Klemola T, Tanhuanpää M, Korpimäki E, Ruohomäki K (2002) Specialist and generalist natural enemies as an explanation for geographical gradients in population cycles of northern herbivores. Oikos 99:83–94CrossRefGoogle Scholar
  34. Klemola T, Pettersen T, Stenseth NC (2003a) Trophic interactions in population cycles of voles and lemmings: a model-based synthesis. Adv Ecol Res 33:75–160CrossRefGoogle Scholar
  35. Klemola T, Hanhimäki S, Ruohomäki K, Senn J, Tanhuanpää M, Kaitaniemi P, Ranta H, Haukioja E (2003b) Performance of the cyclic autumnal moth, Epirrita autumnata, in relation to birch mast seeding. Oecologia 135:354–361PubMedGoogle Scholar
  36. Klomp H (1966) The dynamics of a field population of the pine looper, Bupalus piniarius L. (Lep., Geom.). Adv Ecol Res 3:207–305Google Scholar
  37. Krebs CJ (1978) A review of the Chitty hypothesis of population regulation. Can J Zool 56:2463–2480Google Scholar
  38. Littell RC, Milliken GA, Stroup WW, Wolfinger RD (1996) SAS system for mixed models. SAS Institute, Cary, N.C.Google Scholar
  39. Martinat PJ (1987) The role of climatic variation and weather in forest insect outbreaks. In: Barbosa P, Schultz JC (eds) Insect outbreaks. Academic, San Diego, Calif., pp 241–268Google Scholar
  40. Mason RR, Beckwith RC, Paul HG (1977) Fecundity reduction during collapse of a Douglas-fir tussock moth outbreak in northeast Oregon. Environ Entomol 6:623–626Google Scholar
  41. Mougeot F, Redpath SM, Leckie F, Hudson PJ (2003a) The effect of aggressiveness on the population dynamics of a territorial bird. Nature 421:737–739CrossRefPubMedGoogle Scholar
  42. Mougeot F, Redpath SM, Moss R, Matthiopoulos J, Hudson PJ (2003b) Territorial behaviour and population dynamics in red grouse Lagopus lagopus scoticus. I. Population experiments. J Anim Ecol 72:1073–1082CrossRefGoogle Scholar
  43. Myers JH (1988) Can a general hypothesis explain population cycles of forest Lepidoptera? Adv Ecol Res 18:179–242Google Scholar
  44. Myers JH (1990) Population cycles of western tent caterpillars: experimental introductions and synchrony of fluctuations. Ecology 71:986–995Google Scholar
  45. Myers JH (1998) Synchrony in outbreaks of forest Lepidoptera: a possible example of the Moran effect. Ecology 79:1111–1117Google Scholar
  46. Neuvonen S, Haukioja E (1991) The effects of inducible resistance in host foliage on birch-feeding herbivores. In: Tallamy DW, Raupp MJ (eds) Phytochemical induction by herbivores. Wiley, New York, pp 277–289Google Scholar
  47. Neuvonen S, Haukioja E, Molarius A (1987) Delayed inducible resistance against a leaf-chewing insect in four deciduous tree species. Oecologia 74:363–369Google Scholar
  48. Neuvonen S, Niemelä P, Virtanen T (1999) Climatic change and insect outbreaks in boreal forests: the role of winter temperatures. Ecol Bull 47:63–67Google Scholar
  49. Neuvonen S, Ruohomäki K, Bylund H, Kaitaniemi P (2001) Insect herbivores and herbivory effects on mountain birch dynamics. In: Wielgolaski FE (ed) Nordic mountain birch ecosystems. (UNESCO, Man and the Biosphere series 27) UNESCO, Paris, pp 207–222Google Scholar
  50. Niemelä P (1979) Topographical delimitation of Oporinia-damages: experimental evidence of the effect of winter temperature. Rep Kevo Subarct Res Stn 15:33–36Google Scholar
  51. Norrdahl K, Korpimäki E (2002) Changes in individual quality during a 3-year population cycle of voles. Oecologia 130:239–249Google Scholar
  52. Nothnagle PJ, Schultz JC (1987) What is a forest pest? In: Barbosa P, Schultz JC (eds) Insect outbreaks. Academic, San Diego, Calif., pp 59–80Google Scholar
  53. Peltonen M, Liebhold AM, Bjørnstad ON, Williams DW (2002) Spatial synchrony in forest insect outbreaks: roles of regional stochasticity and dispersal. Ecology 83:3120–3129Google Scholar
  54. 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
  55. Reeson AF, Wilson K, Gunn A, Hails RS, Goulson D (1998) Baculovirus resistance in the noctuid Spodoptera exempta is phenotypically plastic and responds to population density. Proc R Soc Lond B Biol Sci 265:1787–1791CrossRefGoogle Scholar
  56. Ruohomäki K (1992) Wing size variation in Epirrita autumnata (Lep., Geometridae) in relation to larval density. Oikos 63:260–266Google Scholar
  57. Ruohomäki K (1994) Larval parasitism in outbreaking and non-outbreaking populations of Epirrita autumnata (Lepidoptera, Geometridae). Entomol Fenn 15:27–34Google Scholar
  58. Ruohomäki K, Hanhimäki S, Haukioja E, Iso-Iivari L, Neuvonen S, Niemelä P, Suomela J (1992) Variability in the efficacy of delayed inducible resistance in mountain birch. Entomol Exp Appl 62:107–115Google Scholar
  59. 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
  60. Ruohomäki K, Klemola T, Kaitaniemi P, Käär M (2003) Crowding-induced responses in a geometrid moth revisited: a field experiment. Oikos 103:489–496CrossRefGoogle Scholar
  61. Selås V (1997) Cyclic population fluctuations of herbivores as an effect of cyclic seed cropping of plants: the mast depression hypothesis. Oikos 80:257–268Google Scholar
  62. Selås V, Hogstad O, Andersson G, von Proschwitz T (2001) Population cycles of autumnal moth, Epirrita autumnata, in relation to birch mast seeding. Oecologia 129:213–219CrossRefGoogle Scholar
  63. Stenseth NC (1999) Population cycles in voles and lemmings: density dependence and phase dependence in a stochastic world. Oikos 87:427–461Google Scholar
  64. Sundell J, Norrdahl K (2002) Body size-dependent refuges in voles: an alternative explanation of the Chitty effect. Ann Zool Fenn 39:325–333Google Scholar
  65. Tammaru T (1998) Determination of adult size in a folivorous moth: constraints at instar level? Ecol Entomol 23:80–89CrossRefGoogle Scholar
  66. Tammaru T, Kaitaniemi P, Ruohomäki K (1996a) Realized fecundity in Epirrita autumnata (Lepidoptera: Geometridae): relation to body size and consequences to population dynamics. Oikos 77:407–416Google Scholar
  67. Tammaru T, Ruohomäki K, Saikkonen K (1996b) Components of male fitness in relation to body size in Epirrita autumnata (Lepidoptera, Geometridae). Ecol Entomol 21:185–192Google Scholar
  68. Tenow O (1972) The outbreaks of Oporinia autumnata Bkh. and Operophthera spp. (Lep., Geometridae) in the Scandinavian mountain chain and northern Finland 1862–1968. Zool Bidr Uppsala [Suppl] 2:1–107Google Scholar
  69. Tenow O, Nilssen A (1990) Egg cold hardiness and topoclimatic limitations to outbreaks of Epirrita autumnata in northern Fennoscandia. J Appl Ecol 27:723–734Google Scholar
  70. Turchin P (2003) Complex population dynamics: a theoretical/empirical synthesis. Princeton University Press, Princeton, N.J.Google Scholar
  71. Virtanen T, Neuvonen S, Nikula A (1998) Modelling topoclimatic patterns of egg mortality of Epirrita autumnata (Lepidoptera: Geometridae) with a geographical information system: predictions for current climate and warmer climate scenarios. J Appl Ecol 35:311–322CrossRefGoogle Scholar
  72. Wellington WG (1952) Air-mass climatology of Ontario north of Lake Huron and Lake Superior before outbreaks of the spruce budworm, Choristoneura fumiferana (Clem.), and the forest tent caterpillar, Malacosoma disstria Hbn. (Lepidoptera: Tortricidae; Lasiocampiidae). Can J Zool 30:114–127Google Scholar
  73. Wellington WG (1960) Qualitative changes in natural populations during changes in abundance. Can J Zool 38:289–314Google Scholar
  74. Williams DW, Liebhold AM (1995) Influence of weather on the synchrony of gypsy moth (Lepidoptera, Lymantriidae) outbreaks in New England. Environ Entomol 24:987–995Google Scholar
  75. Wilson K, Reeson AF (1998) Density-dependent prophylaxis: evidence from Lepidoptera-baculovirus interactions? Ecol Entomol 23:100–101CrossRefGoogle Scholar
  76. Wilson PR, Altrock RC, Harvey KL, Martin SF, Snodgrass HB (1988) The extended solar-activity cycle. Nature 333:748–750CrossRefGoogle Scholar
  77. Wilson K, Cotter SC, Reeson AF, Pell JK (2001) Melanism and disease resistance in insects. Ecol Lett 4:637–649CrossRefGoogle Scholar
  78. Zhu JW, Löfstedt C, Philipp P, Francke W, Tammaru T, Haukioja E (1995) A sex-pheromone component novel to the Geometridae identified from Epirrita autumnata. Entomol Exp Appl 75:159–164Google Scholar

Copyright information

© Springer-Verlag 2004

Authors and Affiliations

  • Tero Klemola
    • 1
    Email author
  • Kai Ruohomäki
    • 1
  • Tommi Andersson
    • 1
    • 2
  • Seppo Neuvonen
    • 2
  1. 1.Section of Ecology, Department of BiologyUniversity of TurkuTurkuFinland
  2. 2.Kevo Subarctic Research InstituteUniversity of TurkuTurkuFinland

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