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Spring phenology and the response to global warming in gall-inducing sawflies

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Abstract

The phenological window of opportunity for mating, oviposition and larval development is an important part in the life cycle of gall-inducing sawflies. Spring temperatures play an essential role in the timing of eclosion and host plant leaf flush, which are evolutionarily synchronized. This study investigates important events in spring phenology and timing of eclosion for three sympatric gall-inducing sawfly species (Symphyta: Tenthredinidae: Pontania nivalis, P. glabrifrons and P. arcticornis) at two sites in northern Norway. The rate of development was established by monitoring the time to eclosion at constant temperatures of 9, 15, 23 and 28 °C. There was no significant difference in the lower developmental threshold (2.36 °C) and hour-degree requirement for eclosion (6909 hour-degrees) for the three Pontania species. These two values were used with field and historical temperature data to estimating eclosion over 21 years (1993–2013). The results showed later eclosion dates at the arctic than at subarctic site (mean difference 16 days, range 2–30). There was a highly significant advance of eclosion from 1993 to 2013 in both sites, an evidence of global warming. Adult presence in the subarctic site (field trapping, 2012 and 2013) supported the simulated model used. Measurements of gall size showed continuous gall growth until late August, well ahead of winter hibernation. To conclude, gall-inducing sawflies show large phenological plasticity in timing of eclosion, largely regulated by spring temperature, indicating that they are highly adapted to unpredictable subarctic and arctic climates.

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References

  • Ahas R, Aasa A, Menzel A, Fedotova VG, Scheifinger H (2002) Changes in European spring phenology. Int J Climatol 22:1727–1738

    Article  Google Scholar 

  • Baker CRB (1980) Some problems in using meteorological data in forecast the timing of insect life cycle. EPPO (Eur Mediterr Plant Prot Organ) Bull 10:83–91

    Article  Google Scholar 

  • Barrett RT (2000) The phenology of spring migration to north Norway. Bird Study 49:270–277

    Article  Google Scholar 

  • Barrett RT (2011) Recent response to climate change among migrant birds in northern Norway. Ring Migr 26:83–93

    Article  Google Scholar 

  • Barstad TE, Nilssen AC (2012) Hibernation adaptation and eclosion synchrony in leaf-galling sawflies in subarctic Norway. Polar Biol 35:1097–1103

    Article  Google Scholar 

  • Benson RB (1960) Studies in Pontania (Hym., Tenthredinidae). Bull Brit Mus (Nat Hist) Entomol 8:367–384

    Google Scholar 

  • Benson RB (1962) Holarctic sawflies (Hymenoptera: Symphyta). Bull Brit Mus (Nat Hist) Entomol 12:379–409

    Google Scholar 

  • Craig TP, Itami JK, Price PW (1989) A strong relationship between oviposition preference and larval performance in a shoot-galling sawfly. Ecology 70:1691–1699

    Article  Google Scholar 

  • Dale VH, Joyce LA, McNulty S, Neilson RP, Ayres MP, Flannigan MD, Hanson PJ, Irland LC, Lugo AE, Peterson CJ, Simberloff D, Swanson FJ, Stocks BJ, Wotton BM (2001) Climate change and forest disturbance. Bioscience 51:723–734

    Article  Google Scholar 

  • Danks HV (1987) Insect dormancy: an ecological perspective. Biol Survey Canada, Natl Mus Nat Sci, Ottawa

    Google Scholar 

  • Danks HV (2004) Seasonal adaptations in arctic insects. Integr Comp Biol 44:85–94

    Article  PubMed  Google Scholar 

  • Hänninen H (1990) Modelling bud dormancy release in trees from cool and temperated regions. Acta For Fenn 213:1–47

    Google Scholar 

  • Heide OM (1993) Daylength and thermal time responses of budburst during dormancy release in some northern deciduous trees. Physiol Plant 88:531–540

    Article  Google Scholar 

  • Heikinheimo M, Lappalainen H (1997) Dependence of the flower bud burst of some plant taxa in Finland on effective temperature sum: implications for climate warming. Ann Bot Fenn 34:229–243

    Google Scholar 

  • Henden JA, Ims RA, Yoccoz NG, Sorensen R, Killengreen ST (2011) Population dynamics of tundra voles in relation to configuration of willow thickets in southern arctic tundra. Polar Biol 34:533–540

    Article  Google Scholar 

  • Hjältén J, Roininen H, Danell K, Price PW (2003) Distribution and oviposition preference of galling sawflies in arctic Canada. Polar Biol 26:768–773

    Article  Google Scholar 

  • Hodek I (2002) Controversial aspects of diapause development. Eur J Entomol 99:163–173

    Article  Google Scholar 

  • Hodek I, Hodková M (1988) Multiple role of temperature during insect diapause: a review. Entomol Exp Appl 49:153–165

    Article  Google Scholar 

  • Høgda KA, Tømmervik H, Karlsen SR (2013) Trends in the start of the growing season in Fennoscandia 1982–2011. Remote Sens 5:4304–4318

    Article  Google Scholar 

  • Humble LM (2006) Overwintering adaptation in arctic sawflies (Hymenoptera: Tenthredinidae) and their parasitoids: cold tolerance. Can Entomol 138:59–71

    Article  Google Scholar 

  • Hunter MD (1992) A variable insect–plant interaction: the relationship between tree budburst phenology and population levels of insect herbivores among trees. Ecol Entomol 16:91–95

    Article  Google Scholar 

  • Hunter AF (1993) Gypsy moth population size and the window of opportunity in spring. Oikos 68:531–538

    Article  Google Scholar 

  • Hunter AF, Elkinton JS (2000) Effects of synchrony with host plant on populations of a spring-feeding Lepidopteran. Ecology 81:1248–1261

    Article  Google Scholar 

  • Jepsen JU, Kapari L, Hagen SB, Schott T, Vindstad OPL, Nilssen AC, Ims RA (2011) Rapid northward expansion of forest insect pest attributed to spring phenology matching with sub-Arctic birch. Glob Change Biol 17:2071–2083

    Article  Google Scholar 

  • Jones BC, Despland E (2006) Effect of synchronization with host plant phenology occur early in the larval development of spring folivore. Can J Zool 84:628–633

    Article  Google Scholar 

  • Karlsen SR, Høgda KA, Wielgolaski FE, Tolvanen A, Tømmervik H, Poikolainen J, Kubin E (2009) Growing-season trends in Fennoscandia 1982–2006. Clim Res 39:275–286

    Article  Google Scholar 

  • Knerer G (1993) Life history diversity in sawflies. In: Wagner MR, Raffa KF (eds) Sawfly life history adaptations to woody plants. Academic Press Inc., San Diego, pp 33–59

    Google Scholar 

  • Kopelke J-P (1985) Über die biologie und parasiten der gallenbildenden blattwepsenarten Pontania dolichura (THOMS. 1871), P. vesicator (BREMI 1849) und P. viminalis (L. 1758) (Hymenoptera: Tenthredinidae). Faun ökol Mitt 5:331–344

    Google Scholar 

  • Kopelke J-P (1994) Der Schmarotzerkomplex (Brutparasiten und Parasitoide) der gallenbildenden Pontania-Arten (Insecta: Hymenoptera: Tenthredinidae). Senckenb biol 73:83–133

    Google Scholar 

  • Kopelke J-P (1998) Eiablage-Strategien bei gallenbildenden Arten der Blattwespen-Gattungen Pontania, Euura und Phyllocolpa (Hymenoptera: Tenthredinidae: Nematinae). Entomol Gen 22:251–275

    Article  Google Scholar 

  • Kopelke J-P (1999) Gallenerzeugende Blattwespen Europas—Taxonomische Grundlagen, Biologie und Ökologie (Tenthredinidae: Nematinae: Euura, Phyllocolpa, Pontania). Cour Forsch Inst Senckenberg 212:1–183

    Google Scholar 

  • Kostál V (2006) Eco-physiological phases of insect diapause. J Insect Physiol 52:113–127

    Article  PubMed  Google Scholar 

  • Lappalainen HK, Linkosalo T, Venäläinen A (2008) Long-term trends in spring phenology in a boreal forest in central Finland. Boreal Environ Res 13:303–318

    Google Scholar 

  • Lennartson M, Ögren E (2004) Clonal variation in temperature requirements for budburst and dehardening in Salix species used for biomass production. Scand J For Res 19:295–302

    Article  Google Scholar 

  • Martel J, Kause A (2002) The phenological window of opportunity for early-season birch sawflies. Ecol Entomol 27:302–307

    Article  Google Scholar 

  • Martel J, Hanhimäki S, Kause A, Haukioja E (2001) Diversity of birch sawfly responses to seasonally atypical diets. Entomol Exp Appl 100:301–309

    Article  Google Scholar 

  • Menzel A, Fabian P (1999) Growing season extended in Europe. Nature 397:659

    Article  CAS  Google Scholar 

  • Mopper S (2005) Phenology-how time creates spatial structure in endophagous insect populations. Ann Zool Fenn 42:327–333

    Google Scholar 

  • Morbey YE, Ydenberg RC (2001) Protandrous arrival timing to breeding areas: a review. Ecol Lett 4:663–673

    Article  Google Scholar 

  • Myking T, Heide OM (1995) Dormancy release and chilling requirements of bud burst of latitudinal ecotypes of Betula pendula and B. pubescens. Tree Physiol 15:697–704

    Article  PubMed  Google Scholar 

  • Nilssen AC (1997) Effect of temperature on pupal development and eclosion dates in the reindeer Oestrids Hypoderma tarandi and Cephenemyia trompe (Diptera: Oestridae). Physiol Chem Ecol 26:296–306

    Google Scholar 

  • Nuorteva M (1971) Die Sägewespenfauna (Hym., Symphyta) von Vuohiniemi, Südfinnland. Ann Ent Fenn 37:179–189

    Google Scholar 

  • Nylin S, Wiklund C, Wickman PO, Garcia-Barros E (1993) Absence of trade-offs between sexual size dimorphism and early male emergence in a butterfly. Ecology 74:1414–1427

    Article  Google Scholar 

  • Nyman T (2000) Phylogeny and ecological evolution of gall-inducing sawflies (Hymenoptera: Tenthredinidae). Dissertation, University of Joensuu, Finland

  • Nyman T, Farrell BD, Zinovjev AG, Vikberg V (2006a) Larval habits, host-plant associations, and speciation in nematine sawflies (Hymenoptera : Tenthredinidae). Evolution 60:1622–1637

    Article  PubMed  Google Scholar 

  • Nyman T, Zinovjev AG, Vikberg V, Farrell BD (2006b) Molecular phylogeny of the sawfly subfamily Nematinae (Hymenoptera: Tenthredinidae). Syst Entomol 31:569–583

    Article  Google Scholar 

  • Parmesan C (2006) Ecological and evolutionary responses to recent climatic change. Annu Rev Ecol Evol Syst 37:637–669

    Article  Google Scholar 

  • Pop EW, Oberbauer SF, Starr G (2000) Predicting vegetative bud break in two arctic deciduous shrub species, Salix pulchra and Betula nana. Oecologia 124:176–184

    Article  Google Scholar 

  • Price PW, Ohgushi T, Roininen H, Ishihara M, Craig TP, Tahvanainen J, Ferrier SM (2004) Release of phylogenetic constraints through low resource heterogeneity: the case of gall-inducing sawflies. Ecol Entomol 29:467–481

    Article  Google Scholar 

  • Ring RA, Tesar D (1981) Adaption to cold in Canadian arctic insects. Cryobiology 18:199–211

    Article  CAS  PubMed  Google Scholar 

  • Roininen H, Danell K, Zinovjev A, Vikberg V, Virtanen R (2002) Community structure, survival and mortality factors in arctic populations of Eupontania leaf gallers. Polar Biol 25:605–611

    Google Scholar 

  • Romo CM, Tylianakis JM (2013) Elevated temperature and drought interact to reduce parasitoid effectiveness and suppressing host. PLoS One 8:1–9

    Article  Google Scholar 

  • Saska MM, Kuzovkina YA (2010) Phenological stages of willow (Salix). Ann Appl Biol 156:431–437

    Article  Google Scholar 

  • Saunders DS (2002) Insect clocks, 3rd edn. Elsevier, Amsterdam

    Google Scholar 

  • Singer MC, Parmesan C (2010) Phenological asynchrony between herbivorous insects and their host: signal of climatic change or pre-existing adaptive strategy? Phil Trans R Soc 365:3161–3176

    Article  Google Scholar 

  • Stone GN, Schönrogge K, Atkinson RJ, Bellido D, Pujade-Villar J (2002) The population biology of oak gall wasps (Hymenoptera: Cynipidae). Ann Rev Entomol 47:633–668

    Article  CAS  Google Scholar 

  • Strathdee AT, Bale JS (1998) Life on the edge: insect ecology in arctic environments. Annu Rev Entomol 43:85–106

  • Tauber MJ, Tauber AC, Masaki S (1986) Seasonal adaptations of insects. Oxford University Press, New York

    Google Scholar 

  • Tsarouhas V, Gullberg U, Lagercrantz U (2003) Mapping of quantitative trait loci controlling timing of bud flush in Salix. Hereditas 138:172–178

    Article  PubMed  Google Scholar 

  • Valtonen A, Leinonen R, Pöyry J, Roininen H, Tuomela J, Ayres MP (2014) Is climate warming more consequential towards poles? The phenology of Lepidoptera in Finland. Glob Change Biol 20:16–27

    Article  Google Scholar 

  • Viitasaari M (2002) Sawflies (Hymenoptera, Symphyta) Vol I: a review of the suborder, the Western Palearctic taxa of Xyeloidae and Pamphiliodae. Tremex Press Ltd, Helsinki

    Google Scholar 

  • Virtanen R, Oksanen L, Razzhivin V (1999) Topographical and regional patterns of tundra heath vegetation from northern Fennoscandia to the Taimyr Peninsula. Acta Bot Fenn 167:29–83

    Google Scholar 

  • Volney WJ, Fleming RA (2000) Climatic change and impacts of boreal forest insects. Agric Ecosyst Environ 82:283–294

    Article  Google Scholar 

  • Wagner MR, Raffa KF (1993) Sawfly life history adaptations to woody plants. Academic Press Inc, San Diego

    Google Scholar 

  • Walker DA, Raynolds MK, Daniels FJA, Einarsson E, Elvebakk A, Gould WA, Katenin AE, Kholod SS, Markson CJ, Melnikov ES, Moskalenko NG, Talbot SS, Yurtsev BA (2005) The circumpolar arctic vegetation map. J Veg Sci 16:267–282

    Article  Google Scholar 

  • Worner SP (1992) Performance of phenological models under variable temperature regimes: consequences of the Kaufmann or rate summation effect. Environ Entomol 21:689–699

    Article  Google Scholar 

  • Zinovjev AG (1993) Subgenera and Palearctic species groups of the genus Pontania, with notes on the taxonomy of some European species of the viminalis-group (Hymenoptera: Tenthredinidae). Zoosyst Ross 2:145–154

    Google Scholar 

  • Zinovjev AG, Vikberg V (1998) On the biology of Nematinae with hiding larvae. Beitr Ent 48:145–155

    Google Scholar 

Download references

Acknowledgments

We are grateful to the “EcoFinn” project at The Arctic University of Norway for lending us the temperature loggers and the use of temperature data from this project. Thanks to Rob Barett for improving the language. The study was funded by Tromsø University Museum.

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Authors and Affiliations

  1. Department of Natural Sciences, Tromsø University Museum, 9037, Tromsø, Norway

    Trond Elling Barstad & Arne C. Nilssen

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  1. Trond Elling Barstad
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  2. Arne C. Nilssen
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Correspondence to Trond Elling Barstad.

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Online Resource 1

Sawfly leaf galls on its willow host: a P. nivalis on S. glauca; b Pontania glabrifrons gall on Salix lanata; c P. arcticornis on S. phylicifolia; and (photos by T. E. Barstad) (TIFF 14072 kb)

Online Resource 2

Study site in Komagdalen, Finnmark. A riparian river plain with willow patches consisting mainly of Salix lanata and S. phylicifolia. Malaise trap on the willow patch at the lower right corner (photo by T. E. Barstad) (TIFF 14402 kb)

Online Resource 3

Study site in Nakkedalen, Troms. A moor stretches through the bottom of the valley with willow patches consisting mainly of Salix spp. and patches of Betula pubescens, which dominate along the hillsides (photo by T. E. Barstad) (TIFF 28806 kb)

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Barstad, T.E., Nilssen, A.C. Spring phenology and the response to global warming in gall-inducing sawflies. Polar Biol 38, 1503–1513 (2015). https://doi.org/10.1007/s00300-015-1712-1

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