Evolutionary Ecology

, Volume 24, Issue 6, pp 1365–1380 | Cite as

Trait means and reaction norms: the consequences of climate change/invasion interactions at the organism level

  • Charlene JanionEmail author
  • Hans Petter Leinaas
  • John S. Terblanche
  • Steven L. Chown
Research Article


How the impacts of climate change on biological invasions will play out at the mechanistic level is not well understood. Two major hypotheses have been proposed: invasive species have a suite of traits that enhance their performance relative to indigenous ones over a reasonably wide set of circumstances; invasive species have greater phenotypic plasticity than their indigenous counterparts and will be better able to retain performance under altered conditions. Thus, two possibly independent, but complementary mechanistic perspectives can be adopted: based on trait means and on reaction norms. Here, to demonstrate how this approach might be applied to understand interactions between climate change and invasion, we investigate variation in the egg development times and their sensitivity to temperature amongst indigenous and introduced springtail species in a cool temperate ecosystem (Marion Island, 46°54′S 37°54′E) that is undergoing significant climate change. Generalized linear model analyses of the linear part of the development rate curves revealed significantly higher mean trait values in the invasive species compared to indigenous species, but no significant interactions were found when comparing the thermal reaction norms. In addition, the invasive species had a higher hatching success than the indigenous species at high temperatures. This work demonstrates the value of explicitly examining variation in trait means and reaction norms among indigenous and invasive species to understand the mechanistic basis of variable responses to climate change among these groups.


Biological invasions Climate change Development rate Phenotypic plasticity Soil arthropod 



We thank Erika Nortje, Heidi Sjursen Konestabo and various members of the Marion Island relief teams for assistance in the field. Bettine Jansen van Vuuren and Angela McGaughran assisted with the COI sequence data and phylogenetic analysis. Janne Bengtsson, Melodie McGeoch and two anonymous referees provided useful comments on a previous version of the ms. The South African National Antarctic Programme provided logistic support. This work was funded partly by a SA-Norway science liaison grant awarded jointly to HPL and SLC. The work forms a contribution to the SCAR EBA Programme.

Supplementary material

10682_2010_9405_MOESM1_ESM.doc (274 kb)
(DOC 274 kb)


  1. Agrawal AA (2001) Phenotypic plasticity in the interactions and evolution of species. Science 294:321–326. doi: 10.1126/science.1060701 CrossRefPubMedGoogle Scholar
  2. Angilletta MJ (2006) Estimating and comparing thermal performance curves. J Thermal Biol 31:541–545. doi: 10.1016/j.jtherbio.2006.06.002 CrossRefGoogle Scholar
  3. Angilletta MJ, Niewiarowski PH, Navas CA (2002) The evolution of thermal physiology in ectotherms. J Thermal Biol 27:249–268. doi: 10.1016/S0306-4565(01)00094-8 CrossRefGoogle Scholar
  4. Angilletta MJ, Wilson RS, Navas CA et al (2003) Tradeoffs and the evolution of thermal reaction norms. Trends Ecol Evol 18:234–240. doi: 10.1016/S0169-5347(03)00087-9 CrossRefGoogle Scholar
  5. Avise JC, Robinson TJ (2008) Hemiplasy: a new term in the lexicon of phylogenetics. Syst Biol 57:503–507. doi: 10.1080/10635150802164587 CrossRefPubMedGoogle Scholar
  6. Baker HG (1965) Characteristics and modes of origin of weeds. In: Baker HG, Stebbins GL (eds) The genetics of colonizing species. Academic Press, New York, pp 147–168Google Scholar
  7. Birkemoe T, Leinaas HP (2000) Effects of temperature on the development of an Arctic Collembola (Hypogastrura tullbergi). Funct Ecol 14:693–700. doi: 10.1046/j.1365-2435.2000.00478.x CrossRefGoogle Scholar
  8. Blackburn TM, Lockwood JL, Cassey P (2009) Avian invasions. The ecology and evolution of exotic birds. Oxford University Press, OxfordCrossRefGoogle Scholar
  9. Brook BW (2008) Synergies between climate change, extinctions and invasive invertebrates. Wildl Res 35:249–252. doi: 10.1071/WR07116 CrossRefGoogle Scholar
  10. Brook BW, Sodhi NS, Bradshaw CJA (2008) Synergies among extinction drivers and global change. Trends Ecol Evol 23:453–460. doi: 10.1016/j.tree.2008.03.011 CrossRefPubMedGoogle Scholar
  11. Cannon RJC (1998) The implications of predicted climate change for insect pests in the UK, with emphasis on non-indigenous species. Global Change Biol 4:785–796. doi: 10.1046/j.1365-2486.1998.00190.x CrossRefGoogle Scholar
  12. Carroll SP, Fox CW (2007) Dissecting the evolutionary impacts of plant invasions: bugs and beetles as native guides. Global Change Biol 13:1644–1657. doi: 10.1111/j.1365-2486.2007.01403.x CrossRefGoogle Scholar
  13. Chown SL, Froneman PW (2008) The Prince Edward Islands. Land–sea interactions in a changing climate. African Sun Media, StellenboschGoogle Scholar
  14. Chown SL, Gaston KJ (2008) Macrophysiology for a changing world. Proc R Soc B 275:1469–1478. doi: 10.1098/rspb.2008.0137 CrossRefPubMedGoogle Scholar
  15. Chown SL, Nicolson SW (2004) Insect physiological ecology. Mechanisms and patterns. Oxford University Press, OxfordCrossRefGoogle Scholar
  16. Chown SL, McGeoch MA, Marshall DJ (2002) Diversity and conservation of invertebrates on the sub-Antarctic Prince Edward Islands. Afr Entomol 10:67–82Google Scholar
  17. Chown SL, Slabber S, McGeoch MA et al (2007) Phenotypic plasticity mediates climate change responses among invasive and indigenous arthropods. Proc R Soc B 274:2661–2667. doi: 10.1098/rspb.2007.0772 CrossRefGoogle Scholar
  18. Cooper J, Condy PR (1988) Environmental conservation at the sub-Antarctic Prince Edward Islands: a review and recommendations. Environ Conserv 15:317–326CrossRefGoogle Scholar
  19. Daehler CC (2003) Performance comparisons of co-occurring native and alien invasive plants: implications for conservation and restoration. Ann Rev Ecol Evol Syst 34:183–211. doi: 10.1146/annurev.ecolsys.34.011802.132403 CrossRefGoogle Scholar
  20. David JR, Gibert P, Gravot E et al (1997) Phenotypic plasticity and developmental temperature in Drosophila: analysis and significance of reaction norms of morphometrical traits. J Thermal Biol 22:441–451. doi: 10.1016/S0306-4565(97)00063-6 CrossRefGoogle Scholar
  21. Davis MB, Shaw RG (2001) Range shifts and adaptive responses to quaternary climate change. Science 292:673–679. doi: 10.1126/science.292.5517.673 CrossRefPubMedGoogle Scholar
  22. de Jong G (1995) Phenotypic plasticity as a product of selection in a variable environment. Am Nat 145:493–512. doi: 10.1086/285752 CrossRefGoogle Scholar
  23. de Jong G (2005) Evolution of phenotypic plasticity: patterns of plasticity and the emergence of ecotypes. New Phytol 166:101–118CrossRefPubMedGoogle Scholar
  24. de Jong G, van der Have TM (2008) Temperature dependence of development rate, growth rate and size: from biophysics to adaptation. In: Whitman DW, Ananthakrishnan TN (eds) Phenotypic plasticity of insects: mechanisms and consequence. Science, Enfield, pp 461–526Google Scholar
  25. de Mazancourt C, Johnson E, Barraclough TG (2008) Biodiversity inhibits species’ evolutionary responses to changing environments. Ecol Lett 11:380–388. doi: 10.1111/j.1461-0248.2008.01152.x CrossRefPubMedGoogle Scholar
  26. Deere JA, Chown SL (2006) Testing the beneficial acclimation hypothesis and its alternatives for locomotor performance. Am Nat 168:630–644. doi: 10.1086/508026 CrossRefPubMedGoogle Scholar
  27. Deharveng L (1981) Collemboles des iles subantarctiques de l’Océan Indien Mission J. Travé 1972–1973. Comité National Française des Recherches Antarctiques 48:33–108Google Scholar
  28. Deutsch CA, Tewksbury JJ, Huey RB et al (2008) Impacts of climate warming on terrestrial ectotherms across latitude. Proc Natl Acad Sci USA 105:6668–6672. doi: 10.1073/pnas.0709472105 CrossRefPubMedGoogle Scholar
  29. Diamond JM (1989) Overview of recent extinctions. In: Western D, Pearl MC (eds) Conservation for the twenty-first century. Oxford University Press, Oxford, pp 37–41Google Scholar
  30. Didham RK, Tylianakis JM, Gemmell NJ et al (2007) Interactive effects of habitat modification and species invasion on native species decline. Trends Ecol Evol 22:489–496. doi: 10.1016/j.tree.2007.07.001 CrossRefPubMedGoogle Scholar
  31. Dukes J, Mooney HA (1999) Does global change increase the success of biological invaders? Trends Ecol Evol 14:135–139. doi: 10.1016/S0169-5347(98)01554-7 CrossRefPubMedGoogle Scholar
  32. Duncan RP, Blackburn TM, Sol D (2003) The ecology of bird introductions. Annu Rev Ecol Evol Syst 34:71–98. doi: 10.1146/annurev.ecolsys.34.011802.132353 CrossRefGoogle Scholar
  33. Dybdahl MF, Kane SL (2005) Adaptation vs. phenotypic plasticity in the success of a clonal invader. Ecology 86:1592–1601. doi: 10.1890/04-0898 CrossRefGoogle Scholar
  34. Dzialowski AR, Lennon JT, O’Brien WJ et al (2003) Predator-induced phenotypic plasticity in the exotic cladoceran Daphnia lumholtzi. Freshw Biol 48:1593–1602. doi: 10.1046/j.1365-2427.2003.01111.x CrossRefGoogle Scholar
  35. Elton CS (1958) The ecology of invasions by animals and plants. Methuen, LondonGoogle Scholar
  36. Fjellberg A (1998) Fauna Entomologica Scandinavica Volume 35. The Collembola of Fennoscandia and Denmark. Part I: Poduromorpha. Brill, LeidenGoogle Scholar
  37. Frazier MR, Huey RB, Berrigan D (2008) Thermodynamics constrains the evolution of insect population growth rates: “warmer is better”. Am Nat 168:512–520. doi: 10.1086/285797 CrossRefGoogle Scholar
  38. Frenot Y, Chown SL, Whinam J et al (2005) Biological invasions in the Antarctic: extent, impacts and implications. Biol Rev 80:45–72. doi: 10.1017/S1464793104006542 CrossRefPubMedGoogle Scholar
  39. Gabriel AGA, Chown SL, Barendse J et al (2001) Biological invasions on Southern Ocean islands: the Collembola of Marion Island as a test of generalities. Ecography 24:421–430. doi: 10.1111/j.1600-0587.2001.tb00477.x CrossRefGoogle Scholar
  40. Gaston KJ, Chown SL, Mercer RD (2001) The animal species-body size distribution of Marion Island. Proc Natl Acad Sci USA 98:14493–14496. doi: 10.1073/pnas.251332098 CrossRefPubMedGoogle Scholar
  41. Geister TL, Lorenz MW, Hoffmann KH et al (2009) Energetics of embryonic development: effects of temperature in egg and hatchling composition in a butterfly. J Comp Physiol B 179:87–98. doi: 10.1007/s00360-008-0293-5 CrossRefPubMedGoogle Scholar
  42. Ghalambor CK, McKay JK, Carroll SP et al (2007) Adaptive versus non-adaptive phenotypic plasticity and the potential for contemporary adaptation in new environments. Funct Ecol 21:394–407. doi: 10.1111/j.1365-2435.2007.01283.x CrossRefGoogle Scholar
  43. Gilchrist GW (1996) A quantitative genetic analysis of thermal sensitivity in the locomotor performance curve of Aphidius ervi. Evolution 50:1560–1572CrossRefGoogle Scholar
  44. Halsey LG, Butler PJ, Blackburn TM (2006) A phylogenetic analysis of the allometry of diving. Am Nat 167:276–287. doi: 10.1086/499439 CrossRefPubMedGoogle Scholar
  45. Hobbs RJ, Mooney HA (2005) Invasive species in a changing world: the interactions between global change and invasives. In: Mooney HJ, Mack RN, McNeely JA, Neville LE, Schei PJ, Waage JK (eds) Invasive alien species. A new synthesis. Island Press, Washington, pp 310–331Google Scholar
  46. Holzapfel AM, Vinebrooke RD (2005) Environmental warming increases invasion potential of alpine lake communities by imported species. Global Change Biol 11:2009–2015. doi: 10.1111/j.1365-2486.2005.001057.x Google Scholar
  47. Hopkin S (1997) Biology of the springtails. Insecta: Collembola. Oxford University Press, OxfordGoogle Scholar
  48. Hugo EA, McGeoch MA, Marshall DJ et al (2004) Fine scale variation in microarthropod communities inhabiting the keystone species Azorella selago on Marion Island. Polar Biol 27:446–473. doi: 10.1007/s00300-004-0614-4 CrossRefGoogle Scholar
  49. Ikemoto T (2005) Intrinsic optimum temperature for development of insects and mites. Environ Entomol 34:1377–1387. doi: 10.1603/0046-225X-34.6.1377 CrossRefGoogle Scholar
  50. Izem R, Kingsolver JG (2005) Variation in continuous reaction norms: quantifying directions of biological interest. Am Nat 166:277–289. doi: 10.1086/431314 CrossRefPubMedGoogle Scholar
  51. Janion C, Worland MR, Chown SL (2009) Assemblage level variation in lower lethal temperature: the role of invasive species on sub-Antarctic Marion Island. Physiol Entomol 34:284–291. doi: 10.1111/j.1365-3032.2009.00689.x CrossRefGoogle Scholar
  52. Kingsolver JG, Huey RB (1998) Evolutionary analyses of morphological and physiological plasticity in thermally variable environments. Am Zool 38:545–560. doi: 10.1093/icb/38.3.545 Google Scholar
  53. Lawton JH, Brown KC (1986) The population and community ecology of invading insects. Phil Trans R Soc B 314:607–617CrossRefGoogle Scholar
  54. le Roux PC, McGeoch MA (2008) Changes in climate extremes, variability and signature on sub-Antarctic Marion Island. Clim Change 86:309–329. doi: 10.1007/s10584-007-9259-y CrossRefGoogle Scholar
  55. Lee CE (2002) Evolutionary genetics of invasive species. Trends Ecol Evol 17:386–391. doi: 10.1016/S0169-5347(01)02405-3 CrossRefGoogle Scholar
  56. Lee CE, Remfert JL, Gelembiuk GW (2003) Evolution of physiological tolerance and performance during freshwater invasions. Integr Comp Biol 43:439–449. doi: 10.1093/icb/43.3.439 CrossRefGoogle Scholar
  57. Lee C, Remfert J, Chang Y-M (2007) Response to selection and evolvability of invasive populations. Genetica 129:179–192. doi: 10.1016/S0169-5347(01)02405-3 CrossRefPubMedGoogle Scholar
  58. Myburgh M, Chown SL, Daniels SR et al (2007) Population structure, propagule pressure, and conservation biogeography in the sub-Antarctic: lessons from indigenous and invasive springtails. Divers Distr 13:143–154. doi: 10.1111/j.1472-4642.2007.00319.x CrossRefGoogle Scholar
  59. Paradis E, Claude J, Strimmer K (2004) APE: analysis of phylogenetics and evolution in R language. Bioinformatics 20:289–290CrossRefPubMedGoogle Scholar
  60. Parmesan C (2007) Influences of species, latitudes and methodologies on estimates of phenological response to global warming. Global Change Biol 13:1860–1872. doi: 10.1111/j.1365-2486.2007.01404.x CrossRefGoogle Scholar
  61. Parr CL, Sinclair BJ, Andersen AN et al (2005) Constraint and competition in assemblages: a cross-continental and modeling approach for ants. Am Nat 165:481–494CrossRefPubMedGoogle Scholar
  62. Potapov M (2001) Synopses on Palaearctic Collembola, volume 3, Isotomidae. In: Dunger W (ed) Staatliches Museum für Naturkunde, GörlitzGoogle Scholar
  63. Quinn GP, Keough MJ (2002) Experimental design and data analysis for biologists. Cambridge University Press, CambridgeGoogle Scholar
  64. Richardson DM, Pyšek P (2006) Plant invasions: merging the concepts of species invasiveness and community invasibility. Progress Phys Geogr 30:409–431. doi: 10.1191/0309133306pp490pr2006 CrossRefGoogle Scholar
  65. Roff DA (2002) Life history evolution. Sinauer Associates, SunderlandGoogle Scholar
  66. Rosecchi E, Thomas F, Crivelli AJ (2001) Can life-history traits predict the fate of introduced species? A case study on two cyprinid fish in southern France. Freshw Biol 46:845–853. doi: 10.1046/j.1365-2427.2001.00715.x CrossRefGoogle Scholar
  67. Rusek J (1998) Biodiversity of Collembola and their functional role in the ecosystem. Biodiv Conserv 7:1207–1219CrossRefGoogle Scholar
  68. Sala OE, Chapin FS, Armesto JJ et al (2000) Global biodiversity scenarios for the year 2100. Science 287:1770–1774. doi: 10.1126/science.287.5459.1770 CrossRefPubMedGoogle Scholar
  69. Scheiner SM (1993) Genetics and evolution of phenotypic plasticity. Ann Rev Ecol Syst 24:35–68. doi: 10.1146/ CrossRefGoogle Scholar
  70. Sibly RM, Calow P (1986) Physiological ecology of animals. An evolutionary approach. Blackwell Scientific Publications, OxfordGoogle Scholar
  71. Slabber S, Worland MR, Leinaas HP et al (2007) Acclimation effects on thermal tolerances of springtails from sub-Antarctic Marion Island: indigenous and invasive species. J Insect Physiol 53:113–125. doi: 10.1016/j.jinsphys.2006.10.010 CrossRefPubMedGoogle Scholar
  72. Stachowicz JJ, Terwin JR, Whitlatch RB et al (2002) Linking climate change and biological invasions: ocean warming facilitates nonindigenous species invasions. Proc Natl Acad Sci USA 99:15497–15500. doi: 10.1073/pnas.242437499 CrossRefPubMedGoogle Scholar
  73. Stearns SC (1992) The evolution of life histories. Oxford University Press, OxfordGoogle Scholar
  74. Stevens M, Greenslade P, Hogg ID et al (2006) Southern Hemisphere springtails: could any have survived glaciation of Antarctica? Mol Biol Evol 23:574–882. doi: 10.1093/molbev/msj073 CrossRefGoogle Scholar
  75. Stillwell RC, Fox CW (2005) Complex patterns of phenotypic plasticity: interactive effects of temperature during rearing and oviposition. Ecology 86:924–934. doi: 10.1890/04-0547 CrossRefGoogle Scholar
  76. Stohlgren TJ, Barnett DT, Jarnevich CS et al (2008) The myth of plant species saturation. Ecol Lett 11:313–322. doi: 10.1111/j.1461-0248.2008.01153.x CrossRefPubMedGoogle Scholar
  77. Swofford DL (2001) PAUP*: Phylogenetic Analysis Using Parsimony (*and other methods). Sinauer Associates, SunderlandGoogle Scholar
  78. Theoharides KA, Dukes JS (2007) Plant invasion across space and time: factors affecting nonindigenous species success during four stages of invasion. New Phytol 176:256–273. doi: 10.1111/j.1469-8137.2007.02207.x CrossRefPubMedGoogle Scholar
  79. Trudgill DL, Honěk A, van Straalen NM (2005) Thermal time: concepts and utility. Ann Appl Biol 146:1–14. doi: 10.1111/j.1744-7348.2005.04088.x CrossRefGoogle Scholar
  80. Trussell GC, Smith LD (2000) Induced defenses in response to an invading crab predator: an explanation of historical and geographic phenotypic change. Proc Natl Acad Sci USA 97:2123–2127. doi: 10.1073/pnas.040423397 CrossRefPubMedGoogle Scholar
  81. van Kleunen M, Fischer M (2005) Constraints on the evolution of adaptive phenotypic plasticity in plants. New Phytol 166:49–60. doi: 10.1111/j.1469-8137.2004.01296.x CrossRefPubMedGoogle Scholar
  82. van Kleunen M, Johnson SD (2007) South African Iridaceae with rapid and profuse seedling emergence are more likely to become naturalized in other regions. J Ecol 95:674–681. doi: 10.1111/j.1365-2745.2007.01250.x CrossRefGoogle Scholar
  83. van Kleunen M, Manning JC, Pasqualetto V et al (2008) Phylogenetically independent associations between autonomous self fertilization and plant invasiveness. Am Nat 171:195–201. doi: 10.1086/525057 CrossRefPubMedGoogle Scholar
  84. van Straalen NM (1994) Adaptive significance of temperature responses in Collembola. Acta Zool Fennica 195:135–142Google Scholar
  85. Via S, Gomulkiewicz R, DeJong G et al (1995) Adaptive phenotypic plasticity: consensus and controversy. Trends Ecol Evol 10:212–217. doi: 10.1016/S0169-5347(00)89061-8 CrossRefGoogle Scholar
  86. Walther G-R, Roques A, Hulme PE et al (2009) Alien species in a warmer world: risks and opportunities. Trends Ecol Evol 24:686–693. doi: 10.1016/j.tree.2009.06.008 CrossRefPubMedGoogle Scholar
  87. Ward NL, Masters GJ (2007) Linking climate change and species invasion: an illustration using insect herbivores. Global Change Biol 13:1605–1615. doi: 10.1111/j.1365-2486.2007.01399.x CrossRefGoogle Scholar
  88. Warren MS, Hill JK, Thomas JA et al (2001) Rapid responses of British butterflies to opposing forces of climate and habitat change. Nature 414:65–69. doi: 10.1038/35102054 CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  • Charlene Janion
    • 1
    Email author
  • Hans Petter Leinaas
    • 2
  • John S. Terblanche
    • 3
  • Steven L. Chown
    • 1
  1. 1.Centre for Invasion Biology, Department of Botany and ZoologyStellenbosch UniversityMatielandSouth Africa
  2. 2.Department of BiologyUniversity of OsloOsloNorway
  3. 3.Department of Conservation Ecology and EntomologyStellenbosch UniversityMatielandSouth Africa

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