Rapid northwards expansion of a forest insect pest attributed to spring phenology matching with sub‐Arctic birch

Species range displacements owing to shifts in temporal associations between trophic levels are expected consequences of climate warming. Climate-induced range expansions have been shown for two irruptive forest defoliators, the geometrids Operophtera brumata and Epirrita autumnata, causing more extensive forest damage in sub-Arctic Fennoscandia. Here, we document a rapid northwards expansion of a novel irruptive geometrid, Agriopis aurantiaria, into the same region, with the aim of providing insights into mechanisms underlying the recent geometrid range expansions and subsequent forest damage. Based on regional scale data on occurrences and a quantitative monitoring of population densities along the invasion front, we show that, since the first records of larval specimens in the region in 1997–1998, the species has spread northwards to approximately 70°N, and caused severe defoliation locally during 2004–2006. Through targeted studies of larval phenology of A. aurantiaria and O. brumata, as well as spring phenology of birch, along meso-scale climatic gradients, we show that A. aurantiaria displays a similar dynamics and development as O. brumata, albeit with a consistent phenological lag of 0.75–1 instar. Experiments of the temperature requirements for egg hatching and for budburst in birch showed that this phenological lag is caused by delayed egg hatching in A. aurantiaria relative to O. brumata. A. aurantiaria had a higher development threshold (LDTA.a.=4.71 °C, LDTO.b.=1.41 °C), and hatched later and in less synchrony with budburst than O. brumata at the lower end of the studied temperature range. We can conclude that recent warmer springs have provided phenological match between A. aurantiaria and sub-Arctic birch which may intensify the cumulative impact of geometrid outbreaks on this forest ecosystem. Higher spring temperatures will increase spring phenological synchrony between A. aurantiaria and its host, which suggests that a further expansion of the outbreak range of A. aurantiaria can be expected.

[1]  T. Tammaru,et al.  Causes of cyclicity of Epirrita autumnata (Lepidoptera, Geometridae): grandiose theory and tedious practice , 2000, Population Ecology.

[2]  L. Kullman.  20th Century Climate Warming and Tree-limit Rise in the Southern Scandes of Sweden , 2001, Ambio.

[3]  N. M. Straalen,et al.  Thermal time – concepts and utility , 2005 .

[4]  H. Rusterholz,et al.  Effects of elevated CO2 on flowering phenology and nectar production of nectar plants important for butterflies of calcareous grasslands , 1998, Oecologia.

[5]  S. Larsson,et al.  A rapid altitudinal range expansion in the pine processionary moth produced by the 2003 climatic anomaly , 2006 .

[6]  P. C. Reid,et al.  Reorganization of North Atlantic Marine Copepod Biodiversity and Climate , 2002, Science.

[7]  M. Willig,et al.  Impacts of extreme weather and climate on terrestrial biota , 2000 .

[8]  David L. Thomson,et al.  UK birds are laying eggs earlier , 1997, Nature.

[9]  Rik Leemans,et al.  Faculty Opinions recommendation of European phenological response to climate change matches the warming pattern. , 2006 .

[10]  M. Luoto,et al.  Species traits explain recent range shifts of Finnish butterflies , 2009 .

[11]  Stein Rune Karlsen,et al.  Monitoring the spatio-temporal dynamics of geometrid moth outbreaks in birch forest using MODIS-NDVI data , 2009 .

[12]  N. Yoccoz,et al.  Do sub‐Arctic winter moth populations in coastal birch forest exhibit spatially synchronous dynamics? , 2004 .

[13]  K. Williamson.  Birds and Climatic Change , 1975 .

[14]  Marcel E Visser,et al.  Climate change and unequal phenological changes across four trophic levels: constraints or adaptations? , 2009, The Journal of animal ecology.

[15]  S. Quegan,et al.  Spring phenology in boreal Eurasia over a nearly century time scale , 2008 .

[16]  Atle Mysterud,et al.  Climate, changing phenology, and other life history traits: Nonlinearity and match–mismatch to the environment , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[17]  A. Menzel,et al.  Spatial and temporal variability of the phenological seasons in Germany from 1951 to 1996 , 2001 .

[18]  Jerald B. Johnson,et al.  Model selection in ecology and evolution. , 2004, Trends in ecology & evolution.

[19]  G. Meehl,et al.  Climate extremes: observations, modeling, and impacts. , 2000, Science.

[20]  C. Perrins,et al.  ⃛temperature and egg-laying trends , 1998, Nature.

[21]  R. Ahas,et al.  Changes in European spring phenology , 2002 .

[22]  J. Peñuelas,et al.  Responses to a Warming World , 2001, Science.

[23]  R. Ahas.  Long-term phyto-, ornitho- and ichthyophenological time-series analyses in Estonia , 1999 .

[24]  F. Rodríguez-Trelles,et al.  Rapid micro-evolution and loss of chromosomal diversity in Drosophila in response to climate warming , 2004, Evolutionary Ecology.

[25]  C. Perrins,et al.  Effects of elevated temperature on multi‐species interactions: the case of Pedunculate Oak, Winter Moth and Tits , 1999 .

[26]  L. Sternberg,et al.  Sea‐Level Rise and the Reduction in Pine Forests in the Florida Keys , 1994 .

[27]  Anne Tolvanen,et al.  Trends in phenology of Betula pubescens across the boreal zone in Finland , 2008, International journal of biometeorology.

[28]  A. Lugo,et al.  Climate Change and Forest Disturbances , 2001 .

[29]  M. Sturm,et al.  Climate change: Increasing shrub abundance in the Arctic , 2001, Nature.

[30]  N. L. Bradley,et al.  Phenological changes reflect climate change in Wisconsin. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[31]  Walter Zucchini,et al.  Model Selection , 2011, International Encyclopedia of Statistical Science.

[32]  O. Hogstad,et al.  Waves and synchrony in Epirrita autumnata/Operophtera brumata outbreaks. I. Lagged synchrony: regionally, locally and among species. , 2007, The Journal of animal ecology.

[33]  D. Winkler,et al.  Climate change has affected the breeding date of tree swallows throughout North America , 1999, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[34]  J. Gibbs,et al.  Climate Warming and Calling Phenology of Frogs near Ithaca, New York, 1900–1999 , 2001 .

[35]  Camille Parmesan,et al.  Climate and species' range , 1996, Nature.

[36]  Marcel E Visser,et al.  Phenology of forest caterpillars and their host trees: the importance of synchrony. , 2007, Annual review of entomology.

[37]  Anne Tolvanen,et al.  Growing-season trends in Fennoscandia 1982–2006, determined from satellite and phenology data , 2009 .

[38]  D. Roy,et al.  The distributions of a wide range of taxonomic groups are expanding polewards , 2006 .

[39]  C. Parmesan,et al.  Poleward shifts in geographical ranges of butterfly species associated with regional warming , 1999, Nature.

[40]  R. Smith.  Vascular plants as bioindicators of regional warming in Antarctica , 1994, Oecologia.

[41]  D. Gutiérrez,et al.  Changes to the elevational limits and extent of species ranges associated with climate change. , 2005, Ecology letters.

[42]  M. Ayres,et al.  Assessing the consequences of global change for forest disturbance from herbivores and pathogens. , 2000, The Science of the total environment.

[43]  W. Gatter.  Zugzeiten und Zugmuster im Herbst: Einfluß des Treibhauseffekts auf den Vogelzug? , 1992, Journal für Ornithologie.

[44]  S. Hawkins,et al.  Seventy years' observations of changes in distribution and abundance of zooplankton and intertidal organisms in the western English Channel in relation to rising sea temperature , 1995 .

[45]  A. Menzel,et al.  Trends in phenological phases in Europe between 1951 and 1996 , 2000, International journal of biometeorology.

[46]  J. Régnière,et al.  Impacts ofClimate Change on Range Expansion by the Mountain Pine Beetle , 2006 .

[47]  A. Fitter,et al.  Rapid Changes in Flowering Time in British Plants , 2002, Science.

[48]  C. Tucker,et al.  Increased plant growth in the northern high latitudes from 1981 to 1991 , 1997, Nature.

[49]  S. Payette,et al.  Reconstruction of tree-line vegetation response to long-term climate change , 1989, Nature.

[50]  P. Brakefield,et al.  Climate and change in clines for melanism in the two–spot ladybird, Adalia bipunctata (Coleoptera: Coccinellidae) , 1998, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[51]  S. Gilman,et al.  CLIMATE‐RELATED CHANGE IN AN INTERTIDAL COMMUNITY OVER SHORT AND LONG TIME SCALES , 1999 .

[52]  Andrea Battisti,et al.  EXPANSION OF GEOGRAPHIC RANGE IN THE PINE PROCESSIONARY MOTH CAUSED BY INCREASED WINTER TEMPERATURES , 2005 .

[53]  C. Thomas,et al.  Birds extend their ranges northwards , 1999, Nature.

[54]  Colin Robertson,et al.  Spatial–temporal analysis of species range expansion: the case of the mountain pine beetle, Dendroctonus ponderosae , 2009 .

[55]  John H. Campbell,et al.  Biological response to climate change on a tropical mountain , 1999, Nature.

[56]  J. Régnière,et al.  Assessing the Impacts of Global Warming on Forest Pest Dynamics , 2022 .

[57]  P. Niemela.  Topographical delimitation of Oporinia-damages: experimental evidence of the effect of winter temperature. , 1979 .

[58]  Ian P. Woiwod,et al.  Climate change impacts on insect management and conservation in temperate regions: can they be predicted? , 2001 .

[59]  N. Yoccoz,et al.  Phenology and abundance in relation to climatic variation in a sub-arctic insect herbivore–mountain birch system , 2005, Oecologia.

[60]  J. K. Hill,et al.  Rapid responses of British butterflies to opposing forces of climate and habitat change , 2001, Nature.

[61]  O. Hoegh‐Guldberg,et al.  Ecological responses to recent climate change , 2002, Nature.

[62]  T. Beebee,et al.  Amphibian breeding and climate , 1995, Nature.

[63]  A. Aptroot,et al.  Long-Term Monitoring in the Netherlands Suggests that Lichens Respond to Global Warming , 2002, The Lichenologist.

[64]  N. Yoccoz,et al.  Climate change and outbreaks of the geometrids Operophtera brumata and Epirrita autumnata in subarctic birch forest: evidence of a recent outbreak range expansion. , 2008, The Journal of animal ecology.

[65]  David B. Roy,et al.  Phenology of British butterflies and climate change , 2000 .

[66]  Jane Uhd Jepsen,et al.  Shifting altitudinal distribution of outbreak zones of winter moth Operophtera brumata in sub‐arctic birch forest: a response to recent climate warming? , 2007 .

[67]  G. Grabherr,et al.  Climate effects on mountain plants , 1994, Nature.

[68]  Terry V. Callaghan,et al.  A new climate era in the sub‐Arctic: Accelerating climate changes and multiple impacts , 2010 .

[69]  O. Tenow,et al.  Egg cold hardiness and topoclimatic limitations to outbreaks of Epirrita autumnata in Northern Fennoscandia. , 1990 .

[70]  J. O H N,et al.  Herbivory in global climate change research: direct effects of rising temperature on insect herbivores , 2001 .

[71]  O. Hoegh‐Guldberg.  Climate change, coral bleaching and the future of the world's coral reefs , 1999 .

[72]  I. Stirling,et al.  Ecological Dynamics Across the Arctic Associated with Recent Climate Change , 2009, Science.

[73]  R. Fleming,et al.  Climate change and impacts of boreal forest insects , 2000 .

[74]  S. Holbrook,et al.  CHANGES IN AN ASSEMBLAGE OF TEMPERATE REEF FISHES ASSOCIATED WITH A CLIMATE SHIFT , 1997 .

[75]  H. Bylund,et al.  Climatic response of budburst in the mountain birch at two areas in northern Fennoscandia and possible responses to global change , 2003 .

[76]  G. Yohe,et al.  A globally coherent fingerprint of climate change impacts across natural systems , 2003, Nature.

[77]  T. Klemola,et al.  Specialist and generalist natural enemies as an explanation for geographical gradients in population cycles of northern herbivores , 2002 .

[78]  R. Moss,et al.  The regional impacts of climate change : an assessment of vulnerability , 1997 .

[79]  Marcel E. Visser,et al.  Warmer springs disrupt the synchrony of oak and winter moth phenology , 2001, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[80]  Population Cycles of the Autumnal Moth in Fennoscandia , 2002 .

[81]  Annette Menzel,et al.  Growing season extended in Europe , 1999, Nature.

[82]  J. Pounds.  Climate and amphibian declines , 2001, Nature.

[83]  A. Honěk.  Geographical variation in thermal requirements for insect development , 2013 .

[84]  H. Bylund.  Climate and the population dynamics of two insect outbreak species in the north , 1999 .

[85]  T. Klemola,et al.  Reversed Impacts by Specialist Parasitoids and Generalist Predators May Explain a Phase Lag in Moth Cycles: A Novel Hypothesis and Preliminary Field Tests , 2009 .

[86]  Toke Thomas Høye,et al.  The effects of phenological mismatches on demography , 2010, Philosophical Transactions of the Royal Society B: Biological Sciences.

[87]  S. Karlsen,et al.  Phase-dependent outbreak dynamics of geometrid moth linked to host plant phenology , 2009, Proceedings of the Royal Society B: Biological Sciences.

[88]  David B. Roy,et al.  A northward shift of range margins in British Odonata , 2005 .

[89]  K. Baker,et al.  Marine Ecosystem Sensitivity to Climate Change , 1999 .

[90]  Bjørn Lomborg,et al.  The Skeptical Environmentalist , 2001 .

[91]  P. Hersteinsson,et al.  Interspecific competition and the geographical distribution of red and arctic foxes Vulpes vulpes and Alopex lagopus , 1992 .