Hostname: page-component-cd9895bd7-jn8rn Total loading time: 0 Render date: 2024-12-28T03:25:14.695Z Has data issue: false hasContentIssue false

Phenological diversity in the interactions between winter moth (Operophtera brumata) larvae and parasitoid wasps in sub-arctic mountain birch forest

Published online by Cambridge University Press:  08 June 2011

O.P.L. Vindstad*
Affiliation:
Department of Arctic and Marine Biology, University of Tromsø, N-9037 Tromsø, Norway
S.B. Hagen
Affiliation:
Department of Arctic and Marine Biology, University of Tromsø, N-9037 Tromsø, Norway Bioforsk Soil and Environment, Svanhovd, N-9925 Svanvik, Norway
J.U. Jepsen
Affiliation:
Department of Arctic and Marine Biology, University of Tromsø, N-9037 Tromsø, Norway NorwegianInstitute for Nature Research, Fram Centre, N-9296 Tromsø, Norway
L. Kapari
Affiliation:
Department of Arctic and Marine Biology, University of Tromsø, N-9037 Tromsø, Norway
T. Schott
Affiliation:
Department of Arctic and Marine Biology, University of Tromsø, N-9037 Tromsø, Norway
R.A. Ims
Affiliation:
Department of Arctic and Marine Biology, University of Tromsø, N-9037 Tromsø, Norway
*
*Authors for correspondence Fax: +47 77646020 E-mail: ole.p.vindstad@uit.no

Abstract

Population cycles of the winter moth (Operophtera brumata) in sub-arctic coastal birch forests show high spatiotemporal variation in amplitude. Peak larval densities range from levels causing little foliage damage to outbreaks causing spatially extensive defoliation. Moreover, outbreaks typically occur at or near the altitudinal treeline. It has been hypothesized that spatiotemporal variation in O. brumata cycle amplitude results from climate-induced variation in the degree of phenological matching between trophic levels, possibly between moth larvae and parasitoids. The likelihood of mismatching phenologies between larvae and parasitoids is expected to depend on how specialized parasitoids are, both as individual species and as a guild, to attacking specific larval developmental stages (i.e. instars). To investigate the larval instar-specificity of parasitoids, we studied the timing of parasitoid attacks relative to larval phenology. We employed an observational study design, with sequential sampling over the larval period, along an altitudinal gradient harbouring a pronounced treeline outbreak of O. brumata. Within the larval parasitoid guild, containing seven species groups, the timing of attack by different groups followed a successional sequence throughout the moth's larval period and each group attacked 1–2 instars. Such phenological diversity within parasitoid guilds may lower the likelihood of climate-induced trophic mismatches between victim populations and many/all of their enemies. Parasitism rates declined with increasing altitude for most parasitoid groups and for the parasitoid guild as a whole. However, the observed spatiotemporal parasitism patterns provided no clear evidence for or against altitudinal mismatch between larval and parasitoid phenology.

Type
Research Paper
Copyright
Copyright © Cambridge University Press 2011

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Askew, R.R. & Shaw, M.R. (1986) Parasitoid communities: their size, structure and development. pp. 225265 in Waage, J. & Greathead, D. (Eds) Insect Parasitoids. London, UK, Academic Press.Google Scholar
Beckage, N.E. & Riddiford, L.M. (1978) Developmental interactions between tobacco hornworm Manduca sexta and its Braconid parasite Apanteles congregatus. Entomologia Experimentalis et Applicata 23(2), 139151.CrossRefGoogle Scholar
Benrey, B. & Denno, R.F. (1997) The slow-growth-high-mortality hypothesis: A test using the cabbage butterfly. Ecology 78(4), 987999.Google Scholar
Berryman, A.A. (1996) What causes population cycles of forest Lepidoptera? Trends in Ecology & Evolution 11(1), 2832.CrossRefGoogle ScholarPubMed
Burnham, K.P. & Anderson, D.R. (2002) Model Selection and Multimodel Inference: A Practical Information-Theoretic Approach. 2nd edn. New York, USA, Springer-Verlag.Google Scholar
Buse, A., Dury, S.J., Woodburn, R.J.W., Perrins, C.M. & Good, J.E.G. (1999) Effects of elevated temperature on multi-species interactions: the case of Pedunculate Oak, Winter Moth and Tits. Functional Ecology 13, 7482.CrossRefGoogle Scholar
Bylund, H. (1999) Climate and the population dynamics of two insect outbreak species in the north. Ecological Bulletins 47, 5462.Google Scholar
Dijkerman, H.J. (1990) Suitability of eight Yponemeuta species as hosts of Diadegma armilata. Entomologia Experimentalis et Applicata 54(2), 173180.CrossRefGoogle Scholar
Duffy, J.E. (2009) Why biodiversity is important to the functioning of real-world ecosystems. Frontiers in Ecology and the Environment 7(8), 437444.CrossRefGoogle Scholar
Fink, U. & Völkl, W. (1995) The effect of abiotic factors on foraging and oviposition success of the aphid parasitoid Aphidus rosae. Oecologia 103(3), 371378.CrossRefGoogle Scholar
Gross, P. (1993) Insect behavioural and morphological defences against parasitoids. Annual Review of Entomology 38, 251273.CrossRefGoogle Scholar
Gu, H. & Dorn, S. (2001) How do wind velocity and light intensity influence host-location success in Cotesia glomerata (Hym., Braconidae)? Journal of Applied Entomology-Zeitschrift fur Angewandte Entomologie 125(3), 115120.Google Scholar
Hagen, S.B., Sørlibråten, O., Ims, R.A. & Yoccoz, N.G. (2006) Density-dependent melanism in winter moth larvae (Lepidoptera: Geometridae): A countermeasure against parasitoids? Environmental Entomology 35(5), 12491253.CrossRefGoogle Scholar
Hagen, S.B., Jepsen, J.U., Ims, R.A. & Yoccoz, N.G. (2007) Shifting altitudinal distribution of outbreak zones of winter moth Operophtera brumata in sub-arctic birch forest: a response to recent climate warming? Ecography 30(2), 299307.Google Scholar
Hagen, S.B., Jepsen, J.U., Schott, T. & Ims, R.A. (2010) Spatially mismatched trophic dynamics: cyclically outbreaking geometrids and their larval parasitoids. Biology Letters 6, 566569.CrossRefGoogle ScholarPubMed
Hance, T., van Baaren, J., Vernon, P. & Boivin, G. (2007) Impact of extreme temperatures on parasitoids in a climate change perspective. Annual Review of Entomology 52, 107126.CrossRefGoogle Scholar
Harvey, J.A. & Strand, M.R. (2002) The developmental strategies of endoparasitoid wasps vary with host feeding ecology. Ecology 83(9), 24392451.CrossRefGoogle Scholar
Hodkinson, I.D. (2005) Terrestrial insects along elevation gradients: species and community responses to altitude. Biological Reviews 80(3), 489513.CrossRefGoogle ScholarPubMed
Hooper, D.U., Chapin, F.S., Ewel, J.J., Hector, A., Inchausti, P., Lavorel, S., Lawton, J.H., Lodge, D.M., Loreau, M., Naeem, S., Schmid, B., Setala, H., Symstad, A.J., Vandermeer, J. & Wardle, D.A. (2005) Effects of biodiversity on ecosystem functioning: A consensus of current knowledge. Ecological Monographs 75(1), 335.CrossRefGoogle Scholar
Ims, R.A., Yoccoz, N.G. & Hagen, S.B. (2004) Do sub-Arctic winter moth populations in coastal birch forest exhibit spatially synchronous dynamics? Journal of Animal Ecology 73(6), 11291136.CrossRefGoogle Scholar
Jenner, W. & Kuhlmann, U. (2006) Significance of host size for a solitary endoparasitoid: A trade-off between fitness parameters. Basic and Applied Ecology 7(5), 461471.CrossRefGoogle Scholar
Jepsen, J.U., Hagen, S.B., Karlsen, S.R. & Ims, R.A. (2009) Phase-dependent outbreak dynamics of geometrid moth linked to host plant phenology. Proceedings of the Royal Society, Series B: Biological Sciences 276(1676), 41194128.Google ScholarPubMed
Kaitaniemi, P. & Ruohomäki, K. (1999) Effects of autumn temperature and oviposition date on timing of larval development and risk of parasitism in a spring folivore. Oikos 84(3), 435442.CrossRefGoogle Scholar
Karlsen, S.R., Solheim, I., Beck, P.S.A., Høgda, K.A., Wielgolaski, F.E. & Tømmervik, H. (2007) Variability of the start of the growing season in Fennoscandia, 1982–2002. International Journal of Biometeorology 51(6), 513524.CrossRefGoogle ScholarPubMed
Klapwijk, M.J., Grobler, B.C., Ward, K. & Wheeler, D. (2010) Influence of experimental warming and shading on host-parasitoid synchrony. Global Change Biology 16(1), 102112.CrossRefGoogle Scholar
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(1), 8394.CrossRefGoogle Scholar
Klemola, T., Klemola, N., Andersson, T. & Ruohomäki, K. (2007) Does immune function influence population fluctuations and level of parasitism in the cyclic geometrid moth? Population Ecology 49(2), 165178.CrossRefGoogle Scholar
Klemola, N., Heisswolf, A., Ammunèt, T., Ruohomäki, K. & Klemola, T. (2009) Reversed impacts by specialist parasitoids and generalist predators may explain a phase lag in moth cycles: a novel hypothesis and preliminary field tests. Annales Zoologici Fennici 46(5), 380393.CrossRefGoogle Scholar
Lu, J.F., Hu, J. & Fu, W.J. (2006) Levels of encapsulation and melanization in two larval instars of Ostrinia furnacalis Guenee (Lep., Pyralidae) during simulation of parasitization by Macrocentrus cingulum Brischke (Hym., Braconidae). Journal of Applied Entomology 130(5), 290296.CrossRefGoogle Scholar
Menon, A., Flinn, P.W. & Dover, B.A. (2002) Influence of temperature on the functional response of Anisopteromalus calandrae (Hymenoptera: Pteromalidae), a parasitoid of Rhyzopertha dominica (Coleoptera: Bostrichidae). Journal of Stored Products Research 38(5), 463469.CrossRefGoogle Scholar
Mjaaseth, R.R., Hagen, S.B., Yoccoz, N.G. & Ims, R.A. (2005) Phenology and abundance in relation to climatic variation in a sub-arctic insect herbivore-mountain birch system. Oecologia 145(1), 5365.CrossRefGoogle Scholar
Nyrop, J.P. & Simmons, G.A. (1986) Temporal and spatial activity patterns of an adult parasitoid, Glypta fumiferanae (Hymenoptera, Ichneumonidae), and their influence on parasitism. Environmental Entomology 15(3), 481487.CrossRefGoogle Scholar
Peterson, N.A. & Nilssen, A.C. (1998) Late autumn eclosion in the winter moth Operophtera brumata: compromise of selective forces in life-cycle timing. Ecological Entomology 23(4), 417426.CrossRefGoogle Scholar
Porter, K. (1983) Multivoltinism in Apanteles bignellii and the influence of weather on synchronization with its host Euphydryas auriania. Entomologia Experimentalis et Applicata 34(2), 155162.CrossRefGoogle Scholar
R Development Core Team (2008) R: A language and environment for statistical computing. Vienna, Austria, R foundation for statistical computing.Google Scholar
Schott, T. (2007) Patterns in population dynamics and parasitation of autumnal moth and winter moth along an altitudinal gradient in coastal sub-arctic birch forest. MSc thesis, Department of Biology, University of Tromsø, Tromsø, Norway.Google Scholar
Schott, T., Hagen, S.B., Ims, R.A. & Yoccoz, N.G. (2010) Are population outbreaks in sub-arctic geometrids terminated by larval parasitoids? Journal of Animal Ecology 79(3), 701708.CrossRefGoogle ScholarPubMed
Shi, Z.H., Liu, S.S. & Li, Y.X. (2002) Cotesia plutellae parasitizing Plutella xylostella: Host-age dependent parasitism and its effect on host development and food consumption. Biocontrol 47(5), 499511.CrossRefGoogle Scholar
Smith, C.L. & Smilowitz, Z. (1976) Growth and development of Pieris rapae larvae parasitized by Apanteles glomeratus. Entomologia Experimentalis et Applicata 19(2), 189195.CrossRefGoogle Scholar
Stireman, J.O., Dyer, L.A., Janzen, D.H., Singer, M.S., Lill, J.T., Marquis, R.J., Ricklefs, R.E., Gentry, G.L., Hallwachs, W., Coley, P.D., Barone, J.A., Greeney, H.F., Connahs, H., Barbosa, P., Morais, H.C. & Diniz, I.R. (2005) Climatic unpredictability and parasitism of caterpillars: Implications of global warming. Proceedings of the National Academy of Sciences of the United States of America 102, 1738417387.CrossRefGoogle ScholarPubMed
Teder, T., Tanhuanpää, M., Henriksson, J., Kaitaniemi, P. & Ruohomäki, K. (2000) Temporal and spatial variation of larval parasitism in non-outbreaking populations of a folivorous moth. Oecologia 123(4), 516524.CrossRefGoogle ScholarPubMed
Tenow, O. (1972) The outbreaks of Oporinia autumnata Bkh. and Operophtera spp. (Lep., Geometridae) in the Scandinavian mountain chain and northern Finland 1862–1968. Zoologiska Bidrag från Uppsala, Supplement 2, 1107.Google Scholar
van Asch, M. & Visser, M.E. (2007) Phenology of forest caterpillars and their host trees: The importance of synchrony. Annual Review of Entomology 52, 3755.CrossRefGoogle ScholarPubMed
Van Nouhuys, S. & Lei, G.C. (2004) Parasitoid-host metapopulation dynamics: the causes and consequences of phenological asynchrony. Journal of Animal Ecology 73(3), 526535.CrossRefGoogle Scholar
Vindstad, O.P.L., Hagen, S.B, Ims, R.A. & Schott, T. (2010) Spatially patterned guild structure in larval parasitoids of cyclically outbreaking winter moth populations. Ecological Entomology 35(4), 456463.CrossRefGoogle Scholar
Visser, M.E., Holleman, L.J.M. & Gienapp, P. (2006) Shifts in caterpillar biomass phenology due to climate change and its impact on the breeding biology of an insectivorous bird. Oecologia 147(1), 164172.CrossRefGoogle ScholarPubMed
Weisser, W.W., Völkl, W. & Hassell, M.P. (1997) The importance of adverse weather conditions for behaviour and population ecology of an aphid parasitoid. Journal of Animal Ecology 66(3), 386400.CrossRefGoogle Scholar
Weseloh, R.M. (1976) Reduced effectiveness of the Gypsy moth Lymantria dispar (Lepidoptera-Lymantridae) parasite Apanteles melanoscelus (Hymenopetar-Braconidae) in Connecticut due to poor seasonal synchronization with its host. Environmental Entomology 5(4), 743746.CrossRefGoogle Scholar
Zamani, A., Talebi, A., Fathipour, Y. & Baniameri, V. (2006) Temperature-dependent functional response of two aphid parasitoids, Aphidius colemani and Aphidius matricariae (Hymenoptera: Aphidiidae), on the cotton aphid. Journal of Pest Science 79(4), 183188.CrossRefGoogle Scholar