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A unifying framework for biological invasions: the state factor model

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Abstract

Biological invasions are a fixture in our landscapes, with consequent losses in endemic biota and shifts in ecosystem function. Despite the historical recognition of exotic species success in novel environs, this phenomenon lacks a holistic-descriptive framework. Recent attempts to explain biological invasions are based largely on identifying the inherent invasive qualities of successful exotic species (i.e., invasiveness), or characterizing the susceptibility of a habitat to an introduced species (i.e., invasibility), with few studies examining their interaction or additional contributing factors (e.g., time since introduction). We propose unifying the ’points of entry’ into biological invasions with a state factor model that incorporates all contributing variables—not just species or habitats—into a quantifiable, factorial model amenable to hypothesis testing. State factors are phenomenological variables describing the state of a system—historically used in soil and vegetation science. Our state factor equation relates any quantifiable property of an invasion (i) as a function of propagule pressure (p), introduced habitat (h), invader autecology (a), source environment (s), and time since introduction (t). By manipulating state factors singly, or in interaction, targeted variation can be related to quantifiable properties of exotic species while controlling, or at minimum accounting for, remaining factors contributing variation to the system. This holistic factor-function paradigm extends research on invasions from beyond the limits imposed by current theory, fosters novel empirical approaches, elucidates knowledge gaps in our understanding of resident invasions, and allows for variable accounting via a factor matrix. Here we briefly outline the ontogeny of state factors in soil and vegetation science, detail our proposed ’phast’ framework for biological invasions, including notation, and examine a case study in state factor utility.

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Abbreviations

BRH:

Biotic Resistance Hypothesis

DH:

Disturbance Hypothesis

EICA:

Evolution of Increased Competitive Ability Hypothesis

ERH:

Enemy Release Hypothesis

FRH:

Fluctuating Resource Hypothesis

NWH:

Novel Weapons Hypothesis

PP:

Propagule Pressure

References

  • Agrawal AA, Ackerley DD, Adler F, et al (2007) Filling key gaps in population and community ecology. Front Ecol Environ 5:145–152

    Article  Google Scholar 

  • Ahlroth P, Alatalo RV, Holopainen A et al (2003) Founder population size and number of source populations enhance colonization success in waterstriders. Oecologia 137:617–620

    Article  PubMed  Google Scholar 

  • Barney JN, DiTommaso A, Weston LA (2005) Differences in invasibility of two contrasting habitats and invasiveness of two mugwort (Artemisia vulgaris) populations. J Appl Ecol 42:567–576

    Article  Google Scholar 

  • Barney J (2006) North American history of two invasive plant species: phytogeographic distribution, dispersal vectors, and multiple introductions. Biol Invasions 8:703–717

    Article  Google Scholar 

  • Blair AC, Wolfe LM (2004) The evolution of an invasive plant: an experimental study with Silene latifolia. Ecology 85:3035–3042

    Article  Google Scholar 

  • Blossey B, Notzold R (1995) Evolution of increased competitive ability in invasive nonindigenous plants: a hypothesis. J Ecol 83:887–889

    Article  Google Scholar 

  • Bossdorf O, Augue H, Lafuma L et al (2005) Phenotypic and genotypic differentiation between native and introduced plant populations. Oecologia 144:1–11

    Article  PubMed  Google Scholar 

  • Buckley YM, Downey PS, Fowler SV et al (2003) Are invasives bigger? A global study of seed size variation in two invasive shrubs. Ecology 84:1434–1440

    Article  Google Scholar 

  • Byers JE, Noonburg EG (2003) Scale dependent effects of biotic resistance to biological invasion. Ecology 84:1428–1433

    Article  Google Scholar 

  • Callaway RM, Aschehoug ET (2000) Invasive plants versus their new and old neighbors: a mechanism for exotic invasion. Science 290:521–523

    Article  PubMed  CAS  Google Scholar 

  • Carpenter D, Cappuccino N (2005) Herbivory, time since introduction and the invasiveness of exotic plants. J Ecol 93:315–321

    Article  Google Scholar 

  • Cassey P, Blackburn TM, Duncan RP et al (2005) Lessons from the establishment of exotic species: a meta-analytical case study using birds. J Anim Ecol 74:250–258

    Article  Google Scholar 

  • Chong GW, Otsuki Y, Stohlgren TJ et al (2006) Evaluating plant invasions from both habitat and plant perspectives. West North Am Nat 66:92–105

    Article  Google Scholar 

  • Colautti RI, Grigorivich IA, MacIsaac HJ (2006) Propagule pressure: a null model for biological invasions. Biol Invasions 8:1023–1037

    Article  Google Scholar 

  • Darwin C (1859) On the origin of species. John Murray, London, England

    Google Scholar 

  • Davis MA, Grime JP, Thompson K (2000) Fluctuating resources in plant communities: a general theory of invasibility. J Ecol 88:528–534

    Article  Google Scholar 

  • Dokuchaev VV (1949–1961) Socheneniya. in. Moskva, Izd-vo Akademii nauk SSSR, Moscow

  • Durka W, Bossdorf O, Prati D, Auge H (2005) Molecular evidence for multiple introductions of garlic mustard (Alliaria petiolata, Brassicaceae) to North America. Mol Ecol 14:1697–1706

    Article  PubMed  Google Scholar 

  • Elton CS (1958) The ecology of invasions by animals and plants. Methuen, London, England

    Google Scholar 

  • Fridley JD, Stachowicz JJ, Naeem S et al (2007) The invasion paradox: reconciling pattern and process in species invasion. Ecology 88:3–17

    Article  PubMed  CAS  Google Scholar 

  • Grigulis K, Sheppard AW, Ash JE et al (2001) The comparative demography of the pasture weed Echium plantagineum between its native and invaded ranges. J Appl Ecol 38:281–290

    Article  Google Scholar 

  • Hallett SG (2006) Dislocation from coevolved relationships: a unifying theory for plant invasion and naturalization? Weed Sci 54:282–290

    CAS  Google Scholar 

  • Hierro JL, Callaway RM (2003) Allelopathy and exotic plant invasion. Plant Soil 256:29–39

    Article  CAS  Google Scholar 

  • Hierro JL, Maron JL, Callaway RM (2005) A biogeographical approach to plant invasions: the importance of studying exotics in their introduced and native range. J Ecol 93:5–15

    Article  Google Scholar 

  • Hobbs RJ, Huenneke LF (1992) Disturbance, diversity, and invasion: implications for conservation. Conserv Biol 6:324–337

    Article  Google Scholar 

  • Huenneke LF, Hamburg SP, Koide R et al (1990) Effects of soil resources on plant invasion and community structure in a California serpentine grassland. Ecology 71:478–491

    Article  Google Scholar 

  • Jenny H (1941) Factors of soil formation: a system of quantitative pedology. McGraw-Hill, New York

    Google Scholar 

  • Jenny H (1946) Arrangement of soil series and types according to functions of soil-forming factors. Soil Sci 61:375–391

    Article  CAS  Google Scholar 

  • Jenny H (1980) The soil resource: origin and behavior. Springer-Verlag, New York

    Google Scholar 

  • Keane RM, Crawley MJ (2002) Exotic plant invasions and the enemy release hypothesis. Trends Ecol Evol 17:164–170

    Article  Google Scholar 

  • Kowarik I (1995) Time lags in biological invasions with regard to the success and failure of alien species. In: Pyesk P, Prach K, Rejmanek M, Wade M (eds) Plant invasions–general aspects and special problems. Academic Publishing, Amsterdam

  • Krupenikov IA (1992) History of soil science: from its inception to the present. Amerind Publishing Co, New Delhi

    Google Scholar 

  • Lockwood JL, Cassey P, Blackburn T (2005) The role of propagule pressure in explaining species invasions. Trends Ecol Evol 20:223–228

    Article  PubMed  Google Scholar 

  • Lonsdale WM (1999) Global patterns of plant invasions and the concept of invasibility. Ecology 80:1522–1536

    Article  Google Scholar 

  • MacCarthur RH, Wilson EO (1967) The theory of island biogeography. Princeton University Press, Princeton

    Google Scholar 

  • Mack RN, Simberloff D, Lonsdale WM, et al (2000) Biotic invasions: causes, epidemiology, global consequences, and control. Ecol Appl 10:689–710

    Article  Google Scholar 

  • Mack RN, Von Holle B, Meyerson LA (2007) Assessing invasive alien species across multiple spatial scales: working globally and locally. Front Ecol Environ 5:217–220

    Article  Google Scholar 

  • Major J (1951) A functional, factorial approach to plant ecology. Ecology 32:392–412

    Article  Google Scholar 

  • Meyerson LA, Mooney MA (2007) Invasive alien species in an era of globalization. Front Ecol Environ 5:199–208

    Article  Google Scholar 

  • Mitchell CE, Agrawal AA, Bever JD et al (2006) Biotic interactions and plant invasions. Ecol Lett 9:726–740

    Article  PubMed  Google Scholar 

  • Mitchell CG, Power AG (2003) Release of invasive plants from fungal and viral pathogens. Nature 421:625–627

    Article  PubMed  CAS  Google Scholar 

  • Nuzzo V (1993) Current and historic distribution of garlic mustard (Alliaria petiolata) in Illinois. Mich Bot 32:23–34

    Google Scholar 

  • Nuzzo V (1999) Invasion pattern of herb garlic mustard (Alliaria petiolata) in high quality forests. Biol Invasions 1:169–179

    Article  Google Scholar 

  • Reichard SH, Hamilton CW (1997) Predicting invasions of woody plants introduced into North America. Conserv Biol 11:193–203

    Article  Google Scholar 

  • Rejmanek M, Richardson DM (1996) What attributes make some plant species more invasive? Ecology 77:1655–1660

    Article  Google Scholar 

  • Rice B (2007) Invasive species data applications and data sharing across the Americas. Front Ecol Environ 5:W15–W16

    Article  Google Scholar 

  • Saltonstall K (2002) Cryptic invasion by a non-native genotype of the common reed, Phragmites australis, into North America. Proc Nat Acad Sci 99:2445–2449

    Article  PubMed  CAS  Google Scholar 

  • Shea K, Chesson P (2002) Community ecology theory as a framework for biological invasions. Trends Ecol Evol 17:170–176

    Article  Google Scholar 

  • Von Holle B, Simberloff D (2005) Ecological resistance to biological invasion overwhelmed by propagule pressure. Ecology 86:3212–3218

    Article  Google Scholar 

References to Appendix 1

  • Anderson RC, Dhillion SS, Kelley TM (1996) Aspects of the ecology of an invasive plant, garlic mustard (Alliaria petiolata), in Central Illinois. Rest Ecol 4:181–191

    Article  Google Scholar 

  • Bossdorf O, Prati D, Auge H, et al (2004a). Reduced competitive ability in an invasive plant. Ecol Lett 7:346–353

    Article  Google Scholar 

  • Bossdorf O, Schroder S, Prati D, et al (2004b) Palatability and tolerance to simulated herbivory in native and introduced populations of Alliaria petiolata (Brassicaceae). Am J Bot 91:856–862

    Google Scholar 

  • Byers DL, Quinn JA (1998) Demographic variation in Alliaria petiolata (Brassicaceae) in four contrasting habitats. J Torrey Bot Soc 125:138–149

    Article  Google Scholar 

  • Cipollini D (2002) Variation in the expression of chemical defenses in Alliaria petiolata (Brassicaceae) in the field and common garden. Am J Bot 89:1422–1430

    CAS  Google Scholar 

  • Cipollini D, Mbagwu J, Barto K, et al (2005) Expression of constitutive and inducible chemical defenses in native and invasive populations of Alliaria petiolata. J Chem Ecol 31:1255–1267

    Article  PubMed  CAS  Google Scholar 

  • Dhillion SS, Anderson RC (1999) Growth and photosynthetic response of first-year garlic mustard (Alliaria petiolata) to varied irradiance. J Torrey Bot Soc 126:9–14

    Article  Google Scholar 

  • Durka W, Bossdorf O, Prati D, et al (2005) Molecular evidence for multiple introductions of garlic mustard (Alliaria petiolata, Brassicaceae) to North America. Mol Ecol 14:1697–1706

    Article  PubMed  Google Scholar 

  • Lewis K, Bazzaz FA, Liao Q, et al (2006) Geographic patterns of herbivory and resource allocation to defense, growth, and reproduction in an invasive biennial, Alliaria petiolata. Oecologia 148:384–395

    Article  PubMed  Google Scholar 

  • Meekins JF, McCarthy BC (1999) Competitive ability of Alliaria petiolata (garlic mustard, Brassicaceae), an invasive, nonindigenous forest herb. Inter J Plant Sci 160:743–752

    Article  Google Scholar 

  • Meekins JF, McCarthy BC (2000) Responses of the biennial forest herb Alliaria petiolata to variation in population density, nutrient addition and light availability. J Ecol 88:447–463

    Article  Google Scholar 

  • Meekins JF, McCarthy BC (2001) Effect of environmental variations on the invasive success of a nonindigenous forest herb. Ecol Appl 11:1336–1348

    Article  Google Scholar 

  • Meekins JF, McCarthy BC (2002) Effect of population density on the demography of an invasive plant (Alliaria petiolata, Brassicaceae) population in a Southeastern Ohio forest. Am Midl Nat 147:256–278

    Article  Google Scholar 

  • Murphy SD (2005) Concurrent management of an exotic species and initial restoration efforts in forests. Rest Ecol 13:584–593

    Article  Google Scholar 

  • Myers C, Anderson RC (2003) Seasonal variation in photosynthetic rates influences success of an invasive plant, garlic mustard (Alliaria petiolata). Am Midl Nat 150:231–245

    Article  Google Scholar 

  • Myers C, Anderson RC, Byers DL (2005) Influence of shading on the growth and leaf photosynthesis of the invasive non-indigenous plant garlic mustard [Alliaria petiolata (M Bieb) Cavara and Grande] grown under simulated late-winter to mid-spring conditions. J Torrey Bot Soc 132:1–10

    Article  Google Scholar 

  • Prati D, Bossdorf O (2004) Allelopathic inhibition of germination by Alliaria petiolata(Brassicaceae). Am J Bot 91:285–288

    Google Scholar 

  • Rebek KA, O’Neil RJ (2005) Impact of simulated herbivory on Alliaria petiolata survival, growth, and reproduction. Biol Control 34:283–289

    Article  Google Scholar 

  • Rebek KA, O’Neil RJ (2006) The effects of natural and manipulated density regimes on Alliaria petiolata survival, growth and reproduction. Weed Res 46:345–352

    Article  Google Scholar 

  • Renwick JAA, Zhang W, Haribal M, et al (2001) Dual chemical barriers protect a plant against different larval stages of an insect. J Chem Ecol 27:1575–1583

    Article  PubMed  CAS  Google Scholar 

  • Roberts KJ, Anderson RC (2001) Effect of garlic mustard [Alliaria petiolata (Bieb Cavara & Grande)] extracts on plants and arbuscular mycorrhizal (AM) fungi. Am Midl Nat 146:146–152

    Article  Google Scholar 

  • Smith GR, Dingfelder HA, Vaala DA (2003) Effect of plant size and density on garlic mustard reproduction. Northeast Nat 10:269–276

    Google Scholar 

  • Stinson KA, Campbell SA, Powell JR, et al (2006) Invasive plant suppresses the growth of native tree seedlings by disrupting belowground mutualisms. PLoS Biol 4:727–731

    Article  CAS  Google Scholar 

  • Susko DJ, Lovett-Doust L (1998) Variable patterns of seed maturation and abortion in Alliaria petiolata (Brassicaceae). Can J Bot 76:1677–1686

    Article  Google Scholar 

  • Susko DJ, Lovett-Doust L (1999) Effects of resource availability, and fruit and ovule position on components of fecundity in Alliaria petiolata (Brassicaceae). New Phytol 144:295–306

    Article  Google Scholar 

  • Susko DJ, Lovett-Doust L (2000a) Patterns of seed mass variation and their effects on seedling traits in Alliaria petiolata (Brassicaceae). Am J Bot 87:56–66

    Article  PubMed  Google Scholar 

  • Susko DJ, Lovett-Doust L (2000b) Plant-size and fruit-position effects on reproductive allocation in Alliaria petiolata (Brassicaceae). Can J Bot 78:1398–1407

    Article  Google Scholar 

  • Vaughn SF, Berhow MA (1999) Allelochemicals isolated from tissues of the invasive weed garlic mustard (Alliaria petiolata). J Chem Ecol 25:2495–2504

    Article  CAS  Google Scholar 

  • Winterer J, Walsh MC, Poddar M, et al (2005) Spatial and temporal segregation of juvenile and mature garlic mustard plants (Alliaria petiolata) in a Central Pennsylvania woodland. Am Midl Nat 153:209–216

    Article  Google Scholar 

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Acknowledgements

We would like to thank members of the DiTommaso and Blossey lab groups, and Michael Dosmann, Doug Soldat, and Jude Maul for being sounding boards and giving critical reviews of previous incarnations of our state factor concept and reviewing earlier drafts of this manuscript. We also would like to thank two reviewers for helpful suggestions. Special thanks to the late Jack Major for his inspiration.

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Correspondence to Jacob N. Barney.

Appendix

Appendix

Appendix 1 Observational (non-manipulative) and experimental (manipulative) studies on garlic mustard (Alliaria petiolata, ALLPE) showing the methods used to investigate the relationship between state factors and population properties (i)

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Barney, J.N., Whitlow, T.H. A unifying framework for biological invasions: the state factor model. Biol Invasions 10, 259–272 (2008). https://doi.org/10.1007/s10530-007-9127-8

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