Polar Biology

, Volume 39, Issue 8, pp 1467–1478 | Cite as

Analysis of trophic interactions reveals highly plastic response to climate change in a tri-trophic High-Arctic ecosystem

  • Lars O. MortensenEmail author
  • Niels Martin Schmidt
  • Toke T. Høye
  • Christian Damgaard
  • Mads C. Forchhammer
Original Paper


As a response to current climate changes, individual species have changed various biological traits, illustrating an inherent phenotypic plasticity. However, as species are embedded in an ecological network characterised by multiple consumer–resource interactions, ecological mismatches are likely to arise when interacting species do not respond homogeneously. The approach of biological networks analysis calls for the use of structural equation modelling (SEM), a multidimensional analytical setup that has proven particularly useful for analysing multiple interactions across trophic levels. Here we apply SEM to a long-term dataset from a High-Arctic ecosystem to analyse how phenological responses across three trophic levels are coupled to snowmelt patterns and how changes may cascade through consumer–resource interactions. Specifically, the model included the effect of snowmelt on a High-Arctic tri-trophic system of flowers, insects and waders (Charadriiformes), with latent factors representing phenology (timing of life history events) and performance (abundance or reproduction success) for each trophic level. The effects derived from the model demonstrated that the time of snowmelt directly affected plant and arthropod phenology as well as the performance of all included trophic levels. Additionally, timing of snowmelt appeared to indirectly influence wader phenology as well as plant, arthropod and wader performance through effects on adjacent trophic levels and lagged effects. The results from the tri-trophic community presented here emphasise that effects of climate on species in consumer–resource systems may propagate through trophic levels.


Arctic ecosystem Trophic interactions Greenland Phenology Performance Trophic mismatch Plants Arthropods Waders Structural equation modelling 



This study has been financed by the ECOGLOBE initiative. Data were obtained from the Greenland Ecosystem Monitoring program. A big “Thanks” goes to Lars Holst Hansen and Jannik Hansen for great field assistance and data help. Additionally, Nicholas Tyler and Ditte Hendrichsen supplied comments and challenging views, which were greatly appreciated.

Compliance with ethical standards

Ethical statement

All procedures performed in studies involving animals were in accordance with the ethical standards of the institution or practice at which the studies were conducted.


  1. Amano T, Freckleton RP, Queenborough SA et al (2014) Links between plant species’ spatial and temporal responses to a warming climate. Proc R Soc B Biol Sci 281:20133017. doi: 10.1098/rspb.2013.3017 CrossRefGoogle Scholar
  2. Bell KL, Bliss LC (1980) Plant reproduction in a high arctic environment. Arct Antarct Alp Res 12:1–10. doi: 10.2307/1550585 CrossRefGoogle Scholar
  3. Berg MP, Kiers ET, Driessen G et al (2010) Adapt or disperse: understanding species persistence in a changing world. Glob Change Biol 16:587–598. doi: 10.1111/j.1365-2486.2009.02014.x CrossRefGoogle Scholar
  4. Bolduc E, Casajus N, Legagneux P et al (2013) Terrestrial arthropod abundance and phenology in the Canadian Arctic: modelling resource availability for Arctic-nesting insectivorous birds. Can Entomol 145:155–170. doi: 10.4039/tce.2013.4 CrossRefGoogle Scholar
  5. Callaghan TV, Bjorn LO, Chernov Y et al (2004) Synthesis of effects in four Arctic subregions. Ambio 33:469–473CrossRefPubMedGoogle Scholar
  6. Cooper EJ, Dullinger S, Semenchuk P (2011) Late snowmelt delays plant development and results in lower reproductive success in the High Arctic. Plant Sci 180:157–167. doi: 10.1016/j.plantsci.2010.09.005 CrossRefPubMedGoogle Scholar
  7. Dullinger S, Gattringer A, Thuiller W et al (2012) Extinction debt of high-mountain plants under twenty-first-century climate change. Nat Clim Change 2:619–622. doi: 10.1038/nclimate1514 CrossRefGoogle Scholar
  8. Elberling B, Tamstorf MP, Michelsen A et al (2008) Soil and plant community-characteristics and dynamics at Zackenberg. Adv Ecol Res 40:223–248. doi: 10.1016/S0065-2504(07)00010-4 CrossRefGoogle Scholar
  9. Forchhammer MC, Post E (2004) Using large-scale climate indices in climate change ecology studies. Popul Ecol 46:1–12. doi: 10.1007/s10144-004-0176-x CrossRefGoogle Scholar
  10. Forchhammer MC, Schmidt NM, Høye TT et al (2008) Population dynamical responses to climate change. Adv Ecol Res 40:391–420. doi: 10.1016/S0065-2504(07)00017-7 CrossRefGoogle Scholar
  11. Forrest JRK, Thomson JD (2011) An examination of synchrony between insect emergence and flowering in Rocky Mountain meadows. Ecol Monogr 81:469–491. doi: 10.1890/10-1885.1 CrossRefGoogle Scholar
  12. Grabowski MM, Doyle FI, Reid DG et al (2013) Do Arctic-nesting birds respond to earlier snowmelt? A multi-species study in north Yukon, Canada. Polar Biol 36:1097–1105. doi: 10.1007/s00300-013-1332-6 CrossRefGoogle Scholar
  13. Grace JB (2006) Structural equation modeling and natural systems. Cambridge University Press, New YorkCrossRefGoogle Scholar
  14. Hair JF, Black WC, Babin BJ, Anderson RE (2010) Applications of SEM. Multivariate data analysis. Pearson, Upper Saddle River, pp 687–783Google Scholar
  15. Hansen J, Schmidt NM, Reneerkens J (2011) Egg hatchability in high Arctic breeding wader species Charadriiformes is not affected by determining incubation stage using the egg flotation technique. Bird Study 58:522–525. doi: 10.1080/00063657.2011.601411 CrossRefGoogle Scholar
  16. Holling CS (1996) Engineering resilience versus ecological resilience. In: Schulze P (ed) Engineering within ecological constraints. The National Academies Press (NAP), Washington, DCGoogle Scholar
  17. Høye TT, Forchhammer MC (2008) Phenology of high-arctic arthropods: effects of climate on spatial, seasonal, and inter-annual variation. Adv Ecol Res 40:299–325. doi: 10.1016/S0065-2504(07)00013-X CrossRefGoogle Scholar
  18. Høye TT, Post E, Meltofte H et al (2007) Rapid advancement of spring in the High Arctic. Curr Biol 17:449–451. doi: 10.1016/j.cub.2007.04.047 CrossRefGoogle Scholar
  19. Høye TT, Post E, Schmidt NM et al (2013) Shorter flowering seasons and declining abundance of flower visitors in a warmer Arctic. Nat Clim Change 3:759–763. doi: 10.1038/nclimate1909 CrossRefGoogle Scholar
  20. Iler AM, Høye TT, Inouye DW, Schmidt NM (2013a) Nonlinear flowering responses to climate: are species approaching their limits of phenological change? Philos Trans R Soc Lond B Biol Sci 368:20120489. doi: 10.1098/rstb.2012.0489 CrossRefPubMedPubMedCentralGoogle Scholar
  21. Iler AM, Inouye DW, Høye TT et al (2013b) Maintenance of temporal synchrony between syrphid flies and floral resources despite differential phenological responses to climate. Glob Change Biol 19:2348–2359. doi: 10.1111/gcb.12246 CrossRefGoogle Scholar
  22. Inouye DW (2008) Effects of climate change on phenology, frost damage, and floral abundance of montane wildflowers. Ecology 89:353–362. doi: 10.1890/06-2128.1 CrossRefPubMedGoogle Scholar
  23. Jonas T, Rixen C, Sturm M, Stoeckli V (2008) How alpine plant growth is linked to snow cover and climate variability. J Geophys Res 113:1–10. doi: 10.1029/2007JG000680 CrossRefGoogle Scholar
  24. Kattsov VM, Källén E (2005) Future climate change: modeling and scenarios for the Arctic. In: Arris L (ed) Arctic climate impact assessment. Cambridge University Press, Cambridge, pp 99–150Google Scholar
  25. Klaassen M, Lindström Å, Meltofte H, Piersma T (2001) Ornithology: Arctic waders are not capital breeders. Nature 413:794–795. doi: 10.1038/35101654 CrossRefPubMedGoogle Scholar
  26. Kline RB (2011) Principles and practice of structural equation modeling, 3rd edn. Guilford Press, New YorkGoogle Scholar
  27. Kline RB (2012) Assumptions in structural equation modeling. In: Hoyle R (ed) Handbook of structural equation modeling. The Guilford Express, New York, pp 111–125Google Scholar
  28. Lenton TM (2012) Arctic climate tipping points. Ambio 41:10–22. doi: 10.1007/s13280-011-0221-x CrossRefPubMedPubMedCentralGoogle Scholar
  29. Macwhiter B, Austin-Smith P, Kroodsma D (2002) Sanderling (Caldris alba). Birds North America
  30. McBean G (2005) Arctic climate: past and present. In: ACIA, Arctic Climate Impact Assessment. ACIA Overview report. Cambridge University Press, Cambridge, pp 21–60Google Scholar
  31. McKinnon L, Picotin M, Bolduc E et al (2012) Timing of breeding, peak food availability, and effects of mismatch on chick growth in birds nesting in the High Arctic. Can J Zool 90:961–971. doi: 10.1139/z2012-064 CrossRefGoogle Scholar
  32. Meltofte H, Rasch M (2008) The study area at Zackenberg. Adv Ecol Res 40:101–110. doi: 10.1016/S0065-2504(07)00005-0 CrossRefGoogle Scholar
  33. Meltofte H, Høye TT, Schmidt NM, Forchhammer MC (2007) Differences in food abundance cause inter-annual variation in the breeding phenology of High Arctic waders. Polar Biol 30:601–606. doi: 10.1007/s00300-006-0219-1 CrossRefGoogle Scholar
  34. Meltofte H, Christensen TR, Elberling B et al (2008a) High-arctic ecosystem dynamics in a changing climate - Ten years of monitoring and research at Zackenberg Research Station, Northeast Greenland - Introduction. Adv Ecol Res 40:1–12. doi: 10.1016/S0065-2504(07)00001-3 CrossRefGoogle Scholar
  35. Meltofte H, Høye TT, Schmidt NM (2008b) Effects of food availability, snow and predation on breeding performance of waders at Zackenberg. Adv Ecol Res 40:325–343. doi: 10.1016/S0065-2504(07)00014-1 CrossRefGoogle Scholar
  36. Miller-Rushing AJ, Høye TT, Inouye DW, Post E (2010) The effects of phenological mismatches on demography. Philos Trans R Soc B Biol Sci 365:3177–3186. doi: 10.1098/rstb.2010.0148 CrossRefGoogle Scholar
  37. Montoya JM, Raffaelli D (2010) Climate change, biotic interactions and ecosystem services. Philos Trans R Soc B Biol Sci 365:2013–2018. doi: 10.1098/rstb.2010.0114 CrossRefGoogle Scholar
  38. Mortensen LO, Jeppesen E, Schmidt NM et al (2014) Temporal trends and variability in a high arctic ecosystem in Greenland: multidimensional analyses of limnic and terrestrial ecosystems. Polar Biol 37:1073–1082. doi: 10.1007/s00300-014-1501-2 CrossRefGoogle Scholar
  39. Nettleship DN (2000) Ruddy turnstone (Arenaria interpres). Birds North Am.
  40. Olesen JM, Bascompte J, Elberling H, Jordano P (2008) Temporal dynamics in a pollination network. Ecology 89:1573–1582. doi: 10.1890/07-0451.1 CrossRefPubMedGoogle Scholar
  41. Overland JE, Wang M, Walsh JE et al (2011) Climate model projections for the Arctic. Snow. Water, Ice and Permafrost in the Arcic. AMAP, pp 1–18Google Scholar
  42. Pace ML, Cole JJ, Carpenter SR, Kitchell JF (1999) Trophic cascades revealed in diverse ecosystems. Trends Ecol Evol 14:483–488CrossRefPubMedGoogle Scholar
  43. Post E, Pedersen C, Wilmers CC, Forchhammer MC (2008) Warming, plant phenology and the spatial dimension of trophic mismatch for large herbivores. Proc R Soc B Biol Sci 275:2005–2013. doi: 10.1098/rspb.2008.0463 CrossRefGoogle Scholar
  44. Post E, Forchhammer MC, Bret-Harte MS et al (2009) Ecological dynamics across the Arctic associated with recent climate change. Science 325:1355–1358. doi: 10.1126/science.1173113 CrossRefPubMedGoogle Scholar
  45. Pugesek BH (2003) Consepts of structural equation modeling in biological research. In: Pugesek BH, Tomer A, Von Eye A (eds) Structural equation modeling: applications in ecological and evolutionary biology. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  46. Root TL, Price JT, Hall KR et al (2003) Fingerprints of global warming on wild animals and plants. Nature 421:57–60. doi: 10.1038/Nature01333 CrossRefPubMedGoogle Scholar
  47. Rosseel Y (2012) lavaan: An R package for structural equation modelingGoogle Scholar
  48. Schmidt NM, Hansen LH, Hansen J et al (2012) BioBasis: Conceptual design and sampling procedures of the biological monitoring programme within Zackenberg Basic. Department of BioScience, Aarhus University, RoskildeGoogle Scholar
  49. Schmitz OJ, Hamback PA, Beckerman AP (2000) Trophic cascades in terrestrial systems: a review of the effects of carnivore removals on plants. Am Nat 155:141–153. doi: 10.1086/303311 CrossRefPubMedGoogle Scholar
  50. Semenchuk P, Elberling B, Cooper EJ (2013) Snow cover and extreme winter warming events control flower abundance of some, but not all species in high arctic Svalbard. Ecol Evol 3:2586–2599CrossRefPubMedPubMedCentralGoogle Scholar
  51. Sharma S, Mukherjee S, Kumar A, Dillon WR (2005) A simulation study to investigate the use of cutoff values for assessing model fit in covariance structure models. J Bus Res 58:935–943. doi: 10.1016/j.jbusres.2003.10.007 CrossRefGoogle Scholar
  52. Sørensen T (1941) Temperature relations and phenology of the northeast Greenland flowering plants. Meddl Gronl 125:1–305. doi: 10.1078/1433-8319-00076 Google Scholar
  53. Strathdee AT, Bale JS (1998) Life on the edge: insect ecology in arctic environments. Annu Rev Entomol 43:85–106CrossRefPubMedGoogle Scholar
  54. Terborgh J, Estes JA (eds) (2010) Trophic cascades : predators, prey, and the changing dynamics of nature. Island Press, Washington, DCGoogle Scholar
  55. Van der Putten WH, Macel M, Visser ME (2010) Predicting species distribution and abundance responses to climate change: why it is essential to include biotic interactions across trophic levels. Philos Trans R Soc B Biol Sci 365:2025–2034. doi: 10.1098/rstb.2010.0037 CrossRefGoogle Scholar
  56. Walther GR (2004) Plants in a warmer world. Perspect Plant Ecol Evol Syst 6:169–185CrossRefGoogle Scholar
  57. Walther GR (2010) Community and ecosystem responses to recent climate change. Philos Trans R Soc B Biol Sci 365:2019–2024. doi: 10.1098/rstb.2010.0021 CrossRefGoogle Scholar
  58. Warnock ND, Gill RE (1996) Dunling (Caldris alpina). In: Birds North Am.Google Scholar
  59. Wheeler HC, Høye TT, Schmidt NM et al (2015) Phenological mismatch with abiotic conditions - implications for flowering in Arctic plants. Ecology 96:775–787. doi: 10.1890/14-0338.1 CrossRefPubMedGoogle Scholar
  60. Zarnetske PL, Skelly DK, Urban MC (2012) Biotic multipliers of climate change. Science 336:1516–1518. doi: 10.1126/science.1222732 CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Lars O. Mortensen
    • 1
    • 2
    Email author
  • Niels Martin Schmidt
    • 2
    • 3
  • Toke T. Høye
    • 2
    • 3
    • 4
  • Christian Damgaard
    • 2
  • Mads C. Forchhammer
    • 5
    • 6
    • 7
  1. 1.Institute for Aquatic ResourcesTechnical University of DenmarkLyngbyDenmark
  2. 2.Department of BioscienceAarhus UniversityAarhusDenmark
  3. 3.Arctic Research Centre (ARC)Aarhus UniversityAarhusDenmark
  4. 4.Aarhus Institute of Advanced SturdiesAarhus UniversityAarhusDenmark
  5. 5.The Polar CentrePenn State UniversityUniversity ParkUSA
  6. 6.Center for Macroecology, Evolution and ClimateUniversity of CopenhagenCopenhagenDenmark
  7. 7.Department of Arctic BiologyThe University Centre of SvalbardLongyearbyenNorway

Personalised recommendations