Cyclic population dynamics of the autumnal moth: biology and importance of parasitic wasps

Our main field sites are located in the northernmost Finland and Norway, where the Kevo Subarctic Research Station (administered by the University of Turku) provides good facilities. Southern, non-outbreaking populations of the autumnal moth are studied in the vicinity of Turku, SW Finland.

The autumnal moth, Epirrita autumnata (Lepidoptera: Geometridae), is a widely distributed and common geometrid throughout most of the Holarctic region. In northern and mountainous parts of Fennoscandia, autumnal moth populations have been shown to display cyclic (with a statistically significant 9–10-year periodicity), high-amplitude fluctuations in densities, which may culminate in devastating outbreak densities for 1–3 successive years. In these areas, the mountain birch (Betula pubescens var. pumila) is the main host for larvae, and vast areas of the subarctic mountain birch zone can be severely damaged, or even killed, during outbreaks. Autumnal moth populations in southern Fennoscandia remain generally at low and stable densities. Recently, winter moth (Operophtera brumata) populations have also reached outbreak densities in Finnish Lapland. Moth larvae hatch in the spring simultaneously with the budding of a host plant. Leaf-chewing larvae feed on foliage through five larval instars, descending from host trees by mid-summer and pupating in the soil. Adults fly in autumn and eggs overwinter.

Our project, focusing on cyclic geometrid defoliators, continues rich tradition of the Department of Biology at the University of Turku. Earlier projects, ever since 1970s, have looked for an explanation for cyclic population dynamics e.g. from intrinsic changes of autumnal moth populations at successive cycle phases and particularly from multifaceted interactions with the main host plant, the mountain birch. However, the working hypothesis of our project suggests that delayed density-dependent mortality due to egg, larval and/or pupal parasitism (introduced by parasitic wasps of the order Hymenoptera) generates the cyclic population dynamics of the autumnal moth. Thus, we concentrate on the parasitism in detail to obtain understanding of the biology of parasitoid species involved in the system. Their two- and three- trophic-level interactions with autumnal moths and mountain birches are examined by large-scale field samplings and by laboratory and field experiments. Together with taxonomists, we also explore taxonomy of these relative poorly known insects.

According to our studies, eggs, larvae and pupae of the autumnal moth are all attacked by hymenopteran parasitoids. We know one true egg parasitoid, belonging to the genus Telenomus (family Scelionidae). Adults of this species are only 0.6–0.7 mm in length. In addition, we have occasionally sampled specimens of a polyembryonic egg-prepupal parasitoid, Copidosoma chalconotum (Encyrtidae).

Larvae of the autumnal moth are attacked by approximately 15 different species. From larval parasitoids, endoparasitoids belonging to families Ichneumonidae and Braconidae are the most commonly met ones. Early-larval parasitoid species, such as braconids Cotesia salebrosa, C. autumnatae, Protapanteles anchisiades, P. immunis and Aleiodes gastritor-agg. as well as ichneumonids Phobocampe sp. typically parasitize on larvae during the third instar and onwards. Late-larval parasitoid species, such as Zele deceptor (Braconidae) and Campoletis varians (Ichneumonidae), attack autumnal moth larvae on their ultimate (5th) or penultimate (4th) instars. As far as we know, the only ectoparasitoid attacking autumnal moth larvae (during 4th and 5th instars) is Eulophus ramicornis (Eulophidae). Furthermore, a larval-pupal parasitoid Agrypon flaveolatum (Ichneumonidae) has been common during the decline phases of the population cycle.

The pupal stage is attacked by approximately 5 different species. The most commonly met species have been ichneumonids Cratichneumon viator, C. rutifrons and Pimpla flavicoxis.

Most parasitoids are potentially generalists, but such a potential may become realized only in southern communities with high enough density of alternative hosts; that is, in the north they are functional specialists having autumnal (and winter) moths as the main hosts. As concluded many times, some sort of delayed density dependence is a prerequisite for a population cycle. Parasitoids as consumers have inevitably a built-in time delay in their numerical response to changes in the host density, fulfilling the condition of delayed density dependence. Our data reveal that during the last outbreak year and especially in the decline phase of a cycle, percentage parasitism of both egg, larval and pupal parasitism can be very high (often > 50%, sometimes > 90%). When the parasitism rates of different developmental stages are calculated as the total percentage parasitism, it is clear that parasitoids must have very strong effect on autumnal moth mortality and population density.

See the recent publication:

Nyman, T., Wutke, S., Koivisto, E., Klemola, T., Shaw, M. R., Andersson, T., Haraldseide, H., Hagen, S. B., Nakadai, R., & Ruohomäki, K. (2022). A curated DNA barcode reference library for parasitoids of northern European cyclically outbreaking geometrid moths. Ecology and Evolution, 12, e9525. https://doi.org/10.1002/ece3.9525

We tested the parasitism hypothesis of moth population cycles by establishing a four-year parasitoid exclusion experiment, with parasitoid-proof exclosures, parasitoid-permeable exclosures and control plots (Klemola N. et al. 2010, Ecology 91: 2506–2513). The exclusion of parasitoids led to high autumnal moth abundances, while the declining abundance in both the parasitoid-permeable exclosures and the control plots paralleled the naturally declining density in the study area and could be explained by high rates of parasitism. Our results provide firm experimental support for the hypothesis that hymenopteran parasitoids have a causal relationship with the delayed density-dependent component required in the generation of autumnal moth population cycles (Klemola N. et al. 2010, Ecology 91: 2506–2513).

In sum, observations on parasitism, together with modeling approaches, have already provided a framework whereby delayed density-dependent mortality due to parasitism is thought of as a driver of regular population cycles of the autumnal moth in northern Fennoscandia. A similar state of affairs prevails for many other cyclic forest lepidopterans. As these previous observations and theoretical studies can now be combined with the first experimental results (Klemola N. et al. 2010, Ecology 91: 2506–2513), the idea of the importance of parasitoids as causal agents in population cycles is further strengthened. We conclude that parasitoids do not merely track autumnal moth densities, but can actually stimulate a dynamic feedback process with their host species. Thus, parasitoids are responsible for the delayed density dependent (i.e., second-order) component of autumnal moth cycles and drive cyclic population dynamics of this forest pest in continental Finnish Lapland.

Our published articles provide more interesting results on autumnal and winter moth population dynamics.

• Nyman, T., Wutke, S., Koivisto, E., Klemola, T., Shaw, M.R., Andersson, T., Haraldseide, H., Hagen, S.B., Nakadai, R. & Ruohomäki, K. 2022: A curated DNA barcode reference library for parasitoids of northern European cyclically outbreaking geometrid moths. – Ecology and Evolution 12: e9525. DOI: 10.1002/ece3.9525
• Klemola, T., Andersson, T. & Ruohomäki, K. 2016: No regulatory role for adult predation in cyclic population dynamics of the autumnal moth, Epirrita autumnata. – Ecological Entomology 41: 582–589. DOI: 10.1111/een.12329
• Fält-Nardmann, J., Klemola, T., Roth, M., Ruohomäki, K. & Saikkonen, K. 2016: Northern geometrid forest pests (Lepidoptera: Geometridae) hatch at lower temperatures than their southern conspecifics: Implications of climate change. – European Journal of Entomology 113: 337–343. DOI: 10.14411/eje.2016.043
• ​Ossipov, V., Klemola, T., Ruohomäki, K. & Salminen J.-P. 2014: Effects of three years’ increase in density of the geometrid Epirrita autumnata on the change in metabolome of mountain birch trees (Betula pubescens ssp. czerepanovii). – Chemoecology 24: 201–214. DOI: 10.1007/s00049-014-0164-3
• Klemola, T., Andersson, T. & Ruohomäki, K. 2014: Delayed density-dependent parasitism of eggs and pupae as a contributor to the cyclic population dynamics of the autumnal moth – Oecologia 175: 1211–1225. DOI: 10.1007/s00442-014-2984-9
• Mäntylä, E., Blande, J.D. & Klemola, T. 2014: Does application of methyl jasmonate to birch mimic herbivory and attract insectivorous birds in nature? – Arthropod-Plant Interactions 8: 143–153. DOI: 10.1007/s11829-014-9296-1
• Ammunét, T., Klemola, T. & Parvinen K. 2014: Consequences of asymmetric competition between resident and invasive defoliators: A novel empirically based modelling approach. – Theoretical Population Biology 92: 107–117. DOI: 10.1016/j.tpb.2013.12.006
• Huttunen, L., Blande, J.D., Li, T., Rousi, M. & Klemola, T. 2013: Effects of warming climate on early-season carbon allocation and height growth of defoliated mountain birches. – Plant Ecology 214: 373–383. DOI: 10.1007/s11258-013-0175-0
• Ruohomäki, K., Klemola, T., Shaw, M.R., Snäll, N., Sääksjärvi, I.E., Veijalainen, A. & Wahlberg, N. 2013: Microgastrinae (Hymenoptera: Braconidae) parasitizing Epirrita autumnata (Lepidoptera: Geometridae) larvae in Fennoscandia with description of Cotesia autumnatae Shaw, sp. n. – Entomologica Fennica 24: 65–80.
• Ammunét, T., Kaukoranta, T., Saikkonen, K., Repo, T. & Klemola, T. 2012: Invasive and resident defoliators in a changing climate: cold tolerance and predictions concerning extreme winter cold as a range-limiting factor. – Ecological Entomology 37: 212–220. DOI: 10.1111/j.1365-2311.2012.01358.x
• Klemola, T., Ammunét, T., Andersson, T., Klemola, N. & Ruohomäki, K. 2012: Larval parasitism rate increases in herbivore-damaged trees: a field experiment with cyclic birch feeding moths. – Oikos 121: 1525–1531. DOI: 10.1111/j.1600-0706.2011.20096.x
• Huttunen, L., Niemelä, P., Ossipov, V., Rousi, M. & Klemola, T. 2012: Do warmer growing seasons ameliorate the recovery of mountain birches after winter moth outbreak? – Trees – Structure and Function 26: 809–819. DOI: 10.1007/s00468-011-0652-9
• Ammunét, T., Klemola, T. & Saikkonen, K. 2011: Impact of host plant quality on geometrid moth expansion on environmental and local population scales. – Ecography 34: 848–855. DOI: 10.1111/j.1600-0587.2011.06685.x
• Klemola, N., Andersson, T., Ruohomäki, K. & Klemola, T. 2010: Experimental test of parasitism hypothesis for population cycles of a forest lepidopteran. – Ecology 91: 2506–2513. DOI: 10.1890/09-2076
• Ammunét, T., Heisswolf, A., Klemola, N. & Klemola, T. 2010: Expansion of the winter moth outbreak range: no restrictive effects of competition with the resident autumnal moth. – Ecological Entomology 35: 45–52. DOI: 10.1111/j.1365-2311.2009.01154.x
• Klemola, T., Kaitaniemi, P. & Ruohomäki, K. 2010: Folivorous larvae on flowers: do autumnal moths benefit from catkins of the mountain birch? – Entomologia Experimentalis et Applicata 134: 60–68. DOI: 10.1111/j.1570-7458.2009.00934.x
• Heisswolf, A., Käär, M., Klemola, T. & Ruohomäki, K. 2010: Local outbreaks of Operophtera brumata and Operophtera fagata cannot be explained by low vulnerability to pupal predation. – Agricultural and Forest Entomology 12: 81–87. DOI: 10.1111/j.1461-9563.2009.00455.x

• Heisswolf, A., Klemola, N., Ammunét, T. & Klemola, T. 2009: Responses of generalist invertebrate predators to pupal densities of autumnal and winter moths under field conditions. – Ecological Entomology 34: 709–717. DOI: 10.1111/j.1365-2311.2009.01121.x
• Klemola, N., Heisswolf, A., Ammunét, 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: 380–393.
• Ammunét, T., Klemola, N., Heisswolf, A. & Klemola, T. 2009: Larval parasitism of the autumnal moth reduces feeding intensity on the mountain birch. – Oecologia 159: 539–547. DOI: 10.1007/s00442-008-1240-6
• Heisswolf, A., Klemola, T., Andersson, T. & Ruohomäki, K. 2009: Shifting body weight-fecundity relationship in a capital breeder: maternal effects on egg numbers of the autumnal moth under field conditions. – Bulletin of Entomological Research 99: 73–81. DOI: 10.1017/S0007485308006135
• Mäntylä, E., Alessio, G.A., Blande, J.D., Heijari, J., Holopainen, J.K., Laaksonen, T., Piirtola, P. & Klemola, T. 2008: From plants to birds: higher avian predation rates in trees responding to insect herbivory. – PLoS ONE 3(7): e2832. DOI: 10.1371/journal.pone.0002832
• Klemola, N., Kapari, L. & Klemola, T. 2008: Host plant quality and defence against parasitoids: no relationship between levels of parasitism and a geometrid defoliator immunoassay. – Oikos 117: 926–934.
• Klemola, T., Andersson, T. & Ruohomäki, K. 2008: Fecundity of the autumnal moth depends on pooled geometrid abundance without a time lag: implications for cyclic population dynamics. – Journal of Animal Ecology 77: 597–604.
• Mäntylä, E., Klemola, T., Sirkiä, P. & Laaksonen, T. 2008: Low light reflectance may explain the attraction of birds to defoliated trees. – Behavioral Ecology 19: 325–330.
• Klemola, N., Klemola, T., Rantala, M. J. & Ruuhola, T. 2007: Natural host-plant quality affects immune defence of an insect herbivore. – Entomologia Experimentalis et Applicata 123: 167–176.
• 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: 165–178.
• Klemola, T., Huitu, O. & Ruohomäki, K. 2006: Geographically partitioned spatial synchrony among cyclic moth populations. – Oikos 114: 349–359.
• Klemola, T., Ruohomäki, K., Andersson, T. & Neuvonen, S. 2004: Reduction in size and fecundity of the autumnal moth, Epirrita autumnata, in the increase phase of a population cycle. – Oecologia 141: 47–56.
• Mäntylä, E., Klemola, T. & Haukioja, E. 2004: Attraction of willow warblers to sawfly-damaged mountain birches: novel function of inducible plant defences? – Ecology Letters 7: 915–918.
• Klemola, T., Hanhimäki, S., Ruohomäki, K., Senn, J., Tanhuanpää, M., Kaitaniemi, P., Ranta, H. & Haukioja, E. 2003: Performance of the cyclic autumnal moth, Epirrita autumnata, in relation to birch mast seeding. – Oecologia 135: 354–361.
• Klemola, T., Ruohomäki, K., Tanhuanpää, M. & Kaitaniemi, P. 2003: Performance of a spring-feeding moth in relation to time of oviposition and bud-burst phenology of different host species. – Ecological Entomology 28: 319–327.
• Ruohomäki, K., Klemola, T., Kaitaniemi, P. & Käär, M. 2003: Crowding-induced responses in a geometrid moth revisited: a field experiment. – Oikos 103: 489–496.
• Tanhuanpää, M., Ruohomäki, K. & Kaitaniemi, P. 2003: Influence of adult and egg predation on reproductive success of Epirrita autumnata (Lepidoptera: Geometridae). – Oikos 102: 263–278.
• 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: 83–94.
• Tanhuanpää, M., Ruohomäki, K., Turchin, P., Ayres, M.P., Bylund, H., Kaitaniemi, P., Tammaru, T. & Haukioja, E. 2002: Population cycles of the autumnal moth in Fennoscandia. Berryman, A.A. (Ed.): Population cycles: the case for trophic interactions. Oxford University Press, New York, pp. 142–154.
• Tanhuanpää, M., Ruohomäki, K. & Uusipaikka, E. 2001: High larval predation rate in non-outbreaking populations of a geometrid moth. – Ecology 82: 281–289.
• Ruohomäki, K., Tanhuanpää, M., Ayres, M.P., Kaitaniemi, P., Tammaru, T. & Haukioja, E. 2000: Causes of cyclicity of Epirrita autumnata (Lepidoptera, Geometridae): grandiose theory and tedious practice. – Population Ecology 42: 211–223.
• 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: 516–524.

• Kaitaniemi, P., Ruohomäki, K., Tammaru, T. & Haukioja, E. 1999: Induced resistance of host tree foliage during and after a natural insect outbreak. – Journal of Animal Ecology 68: 382–389.
• 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. – Journal of Animal Ecology 68: 562–570.
• Ruohomäki, K. 1994: Larval parasitism in outbreaking and non-outbreaking populations of Epirrita autumnata (Lepidoptera, Geometridae). – Entomologica Fennica 15: 27–34.

​Mutualistic interactions between plants and birds: behavioural mechanisms and ecological importance
Mäntylä, Elina (dissertation at 2009-01-17)

Trophic interactions and cyclic population dynamics of the autumnal moth: the importance of hymenopteran parasitoids
Klemola, Netta (dissertation at 2009-05-08)

Trophic interactions of invasive forest herbivores and consequences for the resident ecosystem
Ammunét, Tea (dissertation at 2011-04-29)