Abstract
The success of a biological invasion is context dependent, and yet two key concepts—the invasiveness of species and the invasibility of recipient ecosystems—are often defined and considered separately. We propose a framework that can elucidate the complex relationship between invasibility and invasiveness. It is based on trait-mediated interactions between species and depicts the response of an ecological network to the intrusion of an alien species, drawing on the concept of community saturation. Here, invasiveness of an introduced species with a particular trait is measured by its per capita population growth rate when the initial propagule pressure of the introduced species is very low. The invasibility of the recipient habitat or ecosystem is dependent on the structure of the resident ecological network and is defined as the total width of an opportunity niche in the trait space susceptible to invasion. Invasibility is thus a measure of network instability. We also correlate invasibility with the asymptotic stability of resident ecological network, measured by the leading eigenvalue of the interaction matrix that depicts trait-based interaction intensity multiplied by encounter rate (a pairwise product of propagule pressure of all members in a community). We further examine the relationship between invasibility and network architecture, including network connectance, nestedness and modularity. We exemplify this framework with a trait-based assembly model under perturbations in ways to emulate fluctuating resources and random trait composition in ecological networks. The maximum invasiveness of a potential invader (greatest intrinsic population growth rate) was found to be positively correlated with invasibility of the recipient ecological network. Additionally, ecosystems with high network modularity and high ecological stability tend to exhibit high invasibility. Where quantitative data are lacking we propose using a qualitative interaction matrix of the ecological network perceived by a potential invader so that the structural network stability and invasibility can be estimated from the literature or from expert opinion. This approach links network structure, invasiveness and invasibility in the context of trait-mediated interactions, such as the invasion of insects into mutualistic and antagonistic networks.
Similar content being viewed by others
References
Abrams PA (1983) The theory of limiting similarity. Annu Rev Ecol Syst 14:359–376
Abrams PA (1998) High competition with low similarity and low competition with high similarity: explorative and apparent competition in consumer-resource systems. Am Nat 152:114–128
Allesina S, Tang S (2012) Stability criteria for complex ecosystems. Nature 483:205–208
Bar-Massada A, Kent R, Carmel Y (2014) Environmental heterogeneity affects the location of modelled communities along the niche-neutrality continuum. Proc R Soc B 281:20133249
Bascompte J, Jordano P, Melián CJ, Olesen JM (2003) The nested assembly of plant-animal mutualistic networks. Proc Natl Acad Sci USA 100(16):9383–9387
Bascompte J, Jordano P, Olesen JM (2006) Asymmetric coevolutionary networks facilitate biodiversity maintenance. Science 312:431–433
Bastola UM, Fortuna MA, Pascual-Garcia A, Ferrera A, Bascompte J (2009) The architecture of mutualistic networks minimizes competition and increases biodiversity. Nature 458:1018–1020
Blackburn TM, Pyšek P, Bacher S, Carlton JT, Duncan RP, Jarošík V, Wilson JRU, Richardson DM (2011) A proposed unified framework for biological invasions. Trends Ecol Evol 26:333–339
Blackburn TM, Essl F, Evans T, Hulme PE, Jeschke JM, Kühn I, Kumschick S, Marková Z, Mrugała A, Nentwig W, Pergl J, Pyšek P, Rabitsch W, Ricciardi A, Richardson DM, Sendek A, Vilà M, Wilson JRU, Winter M, Genovesi P, Bacher S (2014) A unified classification of alien species based on the magnitude of their environmental impacts. PLoS Biol 12:e1001850
Brännström A, Loeuille N, Loreau M, Dieckmann U (2011) Emergence and maintenance of biodiversity in an evolutionary food-web model. Theor Ecol 4:467–478
Brose U (2011) Extinctions in complex, size-structured communities. Basic Appl Ecol 12:557–561
Brown PMJ, Ingels B, Wheatley A, Rhule EL, De Clercq P, Van Leeuwen T, Thomas A (2015) Intraguild predation by Harmonia axyridis (Coleoptera: Coccinellidae) on native insects in Europe: molecular detection from field samples. Entomol Sci 18:130–133
Burgos E, Ceva H, Perazzo RPJ, Devoto M, Medan D, Zimmermann M, Delbue AM (2007) Why nestedness in mutualistic networks? J Theor Biol 249:307–313
Chacón J, Landis D, Heimpel G (2008) Potential for biotic interference of a classical biological control agent of the soybean aphid. Biol Control 46:216–225
Chase JM (2005) Towards a really unified theory for metacommunities. Funct Ecol 19:182–186
Clark JS (2012) The coherence problem with the unified neutral theory of biodiversity. Trends Ecol Evol 27:198–202
Claused AM, Newman MEJ (2008) Hierarchical structure and the prediction of missing links in networks. Nature 453:98–101
Darwin CR (1859) On the origin of species. Murray, London
Davis MA, Grime JP, Thompson K (2000) Fluctuating resources in plant communities: a general theory of invasibility. J Ecol 88:528–534
de Visser S, Freymann B, Olff H (2011) The Serengeti food web: empirical quantification and analysis of topological changes under increasing human impact. J Anim Ecol 80:465–475
Donohue I et al (2013) On the dimensionality of ecological stability. Ecol Lett 16:421
Dormann CF, Strauβ R (2014) A method for detecting modules in quantitative bipartite networks. Methods Ecol Evol 5:90–98
Dormann CF, Gruber B, Fruend J (2008) Introducing the bipartite package: analysing ecological networks. R News 8:8–11
Drake JA (1990) The mechanics of community assembly and succession. J Theor Biol 147:213–233
Drossel B, Higgs P, McKane A (2001) The influence of predator-prey population dynamics on the long-term evolution of food web structure. J Theor Biol 208:91–107
Duncan RP, Williams PA (2002) Darwin’s naturalisation hypothesis challenged. Nature 417:608
Dunne JA, Williams RJ, Martinez ND (2002) Network structure and biodiversity loss in food webs: robustness increases with connectance. Ecol Lett 5:558–5657
Eklöf A, Ebenman B (2006) Species loss and secondary extinctions in simple and complex model communities. J Anim Ecol 75:239–246
Estrada E (2007) Topological structural classes of complex networks. Phys Rev E 75:016103
Felix S, Soares AO (2004) Intraguild predation between the aphidophagous ladybird beetles Harmonia axyridis and Coccinella undecimpunctata (Coleoptera : Coccinellidae): the role of body weight. Eur J Entomol 101:237–242
Fridley JD (2011) Biodiversity as a bulwark against invasion: conceptual threads since Elton. In: Richardson DM (ed) Fifty years of invasion ecology: the legacy of Charles Elton. Wiley, Oxford, pp 121–130
Galeano J, Pastor JM, Iriondo JM (2009) Weighted-interaction nestedness estimator (WINE): a new estimator to calculate over frequency matrices. Environ Model Softw 24:1342–1346
Gardiner M, Landis D, Gratton C, DiFonzo C, O’Neal M, Chacon J, Wayo M, Schmidt N, Mueller E, Heimpel G (2009) Landscape diversity enhances biological control of an introduced crop pest in the north-central USA. Ecol Appl 19:143–154
Gilpin ME, Hanski IA (1991) Metapopulation dynamics: empirical and theoretical investigations. Academic Press, London
Guimarães PR et al (2007) Build-up mechanisms determining the topology of mutualistic networks. J Theor Biol 249:181–189
Hautier L, San Martin G, Callier P, de Biseau JC, Grégoire JC (2011) Alkaloids provide evidence of intraguild predation on native coccinellids by Harmonia axyridis in the field. Biol Invas 13:1805–1814
Holland JN, DeAngelis DL (2010) A consumer–resource approach to the density-dependent population dynamics of mutualism. Ecology 91:1286–1295
Hubbell SP (2001) The unified neutral theory of biodiversity and biogeography. Princeton University Press, Princeton
Hui C, Minoarivelo HO, Nuwagaba S, Ramanantoanina A (2015) Adaptive diversification in coevolutionary systems. In: Pontarotti P (ed) Evolutionary biology: biodiversification from genotype to phenotype. Springer, Berlin, pp 167–186
Ingels B, Van Hassel P, Van Leeuwen T, De Clercq P (2015) Feeding history affects intraguild interactions between Harmonia axyridis (Coleoptera: Coccinellidae) and Episyrphus balteatus (Diptera: Syrphidae). PLoS One 10:e0128518
James A, Pitchford JW, Plank MJ (2012) Disentangling nestedness from models of ecological complexity. Nature 487:227–230
Jeffries C (1974) Qualitative stability and digraphs in model ecosystems. Ecology 55:1415–1419
Kiers ET, Palmer TM, Ives AR, Bruno JF, Bronstein JL (2010) Mutualisms in a changing world: an evolutionary perspective. Ecol Lett 13:1459–1474
Kondoh M (2003) Foraging adaptation and the relationship between food-web complexity and stability. Science 299:1388–1391
Loeuille N, Loreau M (2005) Evolutionary emergence of size structured food webs. Proc Natl Acad Sci USA 102:5761–5766
Lonsdale WM (1999) Global patterns of plant invasions and the concept of invasibility. Ecology 80:1522–1536
Loreau M (2000) Are communities saturated? On the relationship between α, β and γ diversity. Ecol Lett 3:73–76
MacArthur RH (1972) Geographical ecology. Harper & Row, New York
May RM (1974) Stability and complexity in model ecosystems. Princeton University Press, Princeton
McCann KS (2000) The diversity-stability debate. Nature 405:228–233
McKane AJ (2004) Evolving complex food webs. Eur Phys J B 38:287–295
Mello MAR et al (2011) The modularity of seed dispersal: differences in structure and robustness between bat and bird-fruit networks. Oecologia 167:131–140
Memmott J, Waser NM, Price MV (2004) Tolerance of pollination networks to species extinctions. Proc R Soc B 271:2605–2611
Minoarivelo HO, Hui C (2016) Trait-mediated interaction leads to structural emergence in mutualistic networks. Evol Ecol 30:105–121
Minoarivelo HO, Hui C, Terblanche JS, Kosakovsky Pond SL, Scheffler K (2014) Detecting phylogenetic signal in mutualistic interaction networks using a Markov process model. Oikos 123:1250–1260
Moravcová L, Pyšek P, Jarošík V, Pergl J (2015) Getting the right traits: reproductive and dispersal characteristics predict the invasiveness of herbaceous plant species. PLoS One 10:e0123634
Morton D, Law R (1997) Regional species pools and the assembly of local ecological communities. J Theor Biol 187:321–331
Newman MEJ (2006) Modularity and community structure in networks. Proc Natl Acad Sci USA 103:8577–8582
Newman MEJ (2010) Networks: an introduction. Oxford University Press, Oxford
Nuwagaba S, Zhang F, Hui C (2015) A hybrid behavioural rule of adaptation and drift explains the emergent architecture of antagonistic networks. Proc R Soc B 282:20150320
Olesen JM, Jordano P (2002) Geographic patterns in plant-pollinator mutualistic networks. Ecology 89:2416–2424
Olesen JM, Bascompte J, Dupont YL, Jordano P (2007) The modularity of pollination networks. Proc Natl Acad Sci 104:19891–19896
Parker GA, Maynard Smith J (1990) Optimality theory in evolutionary biology. Nature 348:27–33
Peacock L, Worner SP (2008) Biological and ecological traits that assist establishment of alien invasive species. NZ Plant Prot 61:1–7
Pell JK, Baverstock J, Roy HE, Ware RL, Majerus MEN (2008) Intraguild predation involving Harmonia axyridis: a review of current knowledge and future perspectives. Biocontrol 53:147–168
Pimm SL, Lawton JH (1978) On feeding on more than one trophic level. Nature 275:542–544
Poisot T (2013) An a posteriori measure of network modularity. F1000 Research 2:130. doi:10.12688/f1000research.2-130.v3
Pyšek P, Richardson DM (2007) Traits associated with invasiveness in alien plants: where do we stand? In: Nentwig W (ed) Biological invasions, ecological studies, vol 193. Springer, Berlin, pp 97–125
Quirk J, Ruppert R (1965) Qualitative economics and the stability of equilibrium. Rev Econ Stud 32:311–326
Raimundo RLG, Gibert JP, Hembry DH, Guimarães PR Jr (2014) Conflicting selection in the course of adaptive diversification: the interplay between mutualism and intraspecific competition. Am Nat 183:363–375
Rezende EL, Lavabre JE, Guimaraes PR Jr, Jordano P, Bascompte J (2007) Non-random coextinctions in phylogenetically structured mutualistic networks. Nature 448:925–928
Richardson DM, Pyšek P (2006) Plant invasions—merging the concepts of species invasiveness and community invasibility. Prog Phys Geograph 30:409–431
Richardson DM, Pyšek P (2012) Naturalization of introduced plants: ecological drivers of biogeographical patterns. New Phytol 196:383–396
Rohr RP, Saavedra S, Bascompte J (2014) On the structural stability of mutualistic systems. Science 345:1253497
Rosenzweig M (1971) The paradox of enrichment. Science 171:385–387
Rosindell J, Hubbell SP, He F, Harmon LJ, Etienne RS (2012) The case for ecological neutral theory. Trends Ecol Evol 27:203–208
Rossberg AG, Brännström Å, Dieckmann U (2010) How trophic interaction strength depends on traits: a conceptual framework for representing multidimensional trophic niche spaces. Theor Ecol 3:13–24
Roy HE, Baverstock J, Ware R, Clark S, Majerus M, Baverstock K, Pell J (2008) Intraguild predation of the aphid pathogenic fungus Pandora neoaphidis by the invasive coccinellid Harmonia axyridis. Ecol Entomol 33:175–182
Roy HE et al (2016) Harmonia axyridis: an inspiration for global collaborations on invasion biology. Biol Invasions. doi:10.1007/s10530-016-1077-6
Santi F, Maini S (2006) Predation upon Adalia bipunctata and Harmonia axyridis eggs by Chrysoperla carnea larvae and Orius laevigatus adults. Bull Insectol 59:53–58
Shea K, Chesson P (2002) Community ecology theory as a framework for biological invasions. Trends Ecol Evol 17:170–176
Stohlgren TJ, Barnett DT, Kartesz J (2003) The rich get richer: patterns of plant invasions in the United States. Front Ecol Environ 1:11–14
Stouffer DB, Bascompte J (2011) Compartmentalisation increases food-web persistence. Proc Natl Acad Sci USA 108:3648–3652
Suweis S, Simini F, Banavar JR, Maritan A (2013) Emergence of structural and dynamical properties of ecological mutualistic networks. Nature 500:449–452
Thébault E, Fontaine C (2010) Stability of ecological communities and the architecture of mutualistic and trophic networks. Sciences 329:853–856
Tilman D (2004) Niche tradeoffs, neutrality, and community structure: a stochastic theory of resource competition, invasion, and community assembly. Proc Natl Acad Sci USA 101:10854–10861
Tylianakis JM, Tscharntke T, Lewis OT (2007) Habitat modification alters the structure of tropical host-parasitoid food webs. Nature 445:202–205
Vacher C, Piou D, Desprez-Loustau M (2008) Architecture of an antagonistic tree/fungus network: the symmetric influence of past evolutionary history. PLoS One 3:e1740
Valdovinos FS, Ramos-Jiliberto R, Garay-Narvaèz L, Urbani P, Dunne JA (2010) Consequences of adaptive behaviour for the structure and dynamics of foodwebs. Ecol Lett 13:1546–1559
van Baalen M, Krivan V, van Rijn PCJ, Sabelis MW (2001) Alternative food, switching predators, and the persistence of predator–prey systems. Am Nat 157:512–524
Ware RL, Yguel B, Majerus MEN (2009) Effects of competition, cannibalism and intra-guild predation on larval development of the European coccinellid Adalia bipunctata and the invasive species Harmonia axyridis. Ecol Entomol 34:12–19
Waxman D, Gavrilets S (2005) 20 questions on adaptive dynamics. J Evol Biol 18:1139–1154
Yodzis P (1981) The stability of real ecosystems. Nature 289:674–676
Zhang F, Hui C, Terblanche JS (2011) An interaction switch predicts the nested architecture of mutualistic networks. Ecol Lett 14:797–803
Acknowledgments
This paper had its origin at a workshop on “Drivers, impacts, mechanisms and adaptation in insect invasions” hosted by the DST-NRF Centre of Excellence for Invasion Biology in Stellenbosch, South Africa, in November 2014. Additional financial support was provided by HortGro, the National Research Foundation of South Africa, Stellenbosch University, and SubTrop. We are grateful to participants at the workshop and to Marc Kenis, Wolfgang Rabitsch, Michael Pocock, Ulf Dieckmann and Åke Brännström for discussions on the concepts presented in this paper. CH is supported by the South African Research Chair Initiative (SARChI), the National Research Foundation of South Africa (Grant nos. 81825 and 76912), and the Australian Research Council (Discovery Project DP150103017). HOM receives a PhD Scholarship from the German Academic Exchange Service (DAAD). HER receives co-funding from the Natural Environment Research Council (NERC) and the Joint Nature Conservation Committee (JNCC). HER also acknowledges the COST Action TD1209. DMR acknowledges support from the National Research Foundation of South Africa (Grant 85417).
Author information
Authors and Affiliations
Corresponding author
Additional information
Guest editors: Matthew P. Hill, Susana Clusella-Trullas, John S. Terblanche & David M. Richardson / Insect Invasions
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Hui, C., Richardson, D.M., Landi, P. et al. Defining invasiveness and invasibility in ecological networks. Biol Invasions 18, 971–983 (2016). https://doi.org/10.1007/s10530-016-1076-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10530-016-1076-7