Abstract
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.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Agrawal AA (2001) Phenotypic plasticity in the interactions and evolution of species. Science 294:321–326. doi:10.1126/science.1060701
Angilletta MJ (2006) Estimating and comparing thermal performance curves. J Thermal Biol 31:541–545. doi:10.1016/j.jtherbio.2006.06.002
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
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
Avise JC, Robinson TJ (2008) Hemiplasy: a new term in the lexicon of phylogenetics. Syst Biol 57:503–507. doi:10.1080/10635150802164587
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 147–168
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
Blackburn TM, Lockwood JL, Cassey P (2009) Avian invasions. The ecology and evolution of exotic birds. Oxford University Press, Oxford
Brook BW (2008) Synergies between climate change, extinctions and invasive invertebrates. Wildl Res 35:249–252. doi:10.1071/WR07116
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
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
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
Chown SL, Froneman PW (2008) The Prince Edward Islands. Land–sea interactions in a changing climate. African Sun Media, Stellenbosch
Chown SL, Gaston KJ (2008) Macrophysiology for a changing world. Proc R Soc B 275:1469–1478. doi:10.1098/rspb.2008.0137
Chown SL, Nicolson SW (2004) Insect physiological ecology. Mechanisms and patterns. Oxford University Press, Oxford
Chown SL, McGeoch MA, Marshall DJ (2002) Diversity and conservation of invertebrates on the sub-Antarctic Prince Edward Islands. Afr Entomol 10:67–82
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
Cooper J, Condy PR (1988) Environmental conservation at the sub-Antarctic Prince Edward Islands: a review and recommendations. Environ Conserv 15:317–326
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
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
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
de Jong G (1995) Phenotypic plasticity as a product of selection in a variable environment. Am Nat 145:493–512. doi:10.1086/285752
de Jong G (2005) Evolution of phenotypic plasticity: patterns of plasticity and the emergence of ecotypes. New Phytol 166:101–118
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 461–526
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
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
Deharveng L (1981) Collemboles des iles subantarctiques de l’Océan Indien Mission J. Travé 1972–1973. Comité National Française des Recherches Antarctiques 48:33–108
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
Diamond JM (1989) Overview of recent extinctions. In: Western D, Pearl MC (eds) Conservation for the twenty-first century. Oxford University Press, Oxford, pp 37–41
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
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
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
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
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
Elton CS (1958) The ecology of invasions by animals and plants. Methuen, London
Fjellberg A (1998) Fauna Entomologica Scandinavica Volume 35. The Collembola of Fennoscandia and Denmark. Part I: Poduromorpha. Brill, Leiden
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
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
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
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
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
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
Gilchrist GW (1996) A quantitative genetic analysis of thermal sensitivity in the locomotor performance curve of Aphidius ervi. Evolution 50:1560–1572
Halsey LG, Butler PJ, Blackburn TM (2006) A phylogenetic analysis of the allometry of diving. Am Nat 167:276–287. doi:10.1086/499439
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 310–331
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
Hopkin S (1997) Biology of the springtails. Insecta: Collembola. Oxford University Press, Oxford
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
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
Izem R, Kingsolver JG (2005) Variation in continuous reaction norms: quantifying directions of biological interest. Am Nat 166:277–289. doi:10.1086/431314
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
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
Lawton JH, Brown KC (1986) The population and community ecology of invading insects. Phil Trans R Soc B 314:607–617
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
Lee CE (2002) Evolutionary genetics of invasive species. Trends Ecol Evol 17:386–391. doi:10.1016/S0169-5347(01)02405-3
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
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
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
Paradis E, Claude J, Strimmer K (2004) APE: analysis of phylogenetics and evolution in R language. Bioinformatics 20:289–290
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
Parr CL, Sinclair BJ, Andersen AN et al (2005) Constraint and competition in assemblages: a cross-continental and modeling approach for ants. Am Nat 165:481–494
Potapov M (2001) Synopses on Palaearctic Collembola, volume 3, Isotomidae. In: Dunger W (ed) Staatliches Museum für Naturkunde, Görlitz
Quinn GP, Keough MJ (2002) Experimental design and data analysis for biologists. Cambridge University Press, Cambridge
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
Roff DA (2002) Life history evolution. Sinauer Associates, Sunderland
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
Rusek J (1998) Biodiversity of Collembola and their functional role in the ecosystem. Biodiv Conserv 7:1207–1219
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
Scheiner SM (1993) Genetics and evolution of phenotypic plasticity. Ann Rev Ecol Syst 24:35–68. doi:10.1146/annurev.es.24.110193.000343
Sibly RM, Calow P (1986) Physiological ecology of animals. An evolutionary approach. Blackwell Scientific Publications, Oxford
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
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
Stearns SC (1992) The evolution of life histories. Oxford University Press, Oxford
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
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
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
Swofford DL (2001) PAUP*: Phylogenetic Analysis Using Parsimony (*and other methods). Sinauer Associates, Sunderland
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
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
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
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
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
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
van Straalen NM (1994) Adaptive significance of temperature responses in Collembola. Acta Zool Fennica 195:135–142
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
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
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
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
Acknowledgments
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.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Janion, C., Leinaas, H.P., Terblanche, J.S. et al. Trait means and reaction norms: the consequences of climate change/invasion interactions at the organism level. Evol Ecol 24, 1365–1380 (2010). https://doi.org/10.1007/s10682-010-9405-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10682-010-9405-2