Skip to main content
SpringerLink
Log in

Instability of a hybrid module of antagonistic and mutualistic interactions

  • Review
  • Published:
Population Ecology

Abstract

Mutualistic and antagonistic interactions coexist in nature. However, little is understood about their relative roles and interactive effects on multispecies coexistence. Here, using a three-species population dynamics model of a resource species, its exploiter, and a mutualist species, we show that a mixture of different interaction types may lead to dynamics that differ completely from those of the isolated interacting pairs. More specifically, a combination of globally stable antagonistic and mutualistic subsystems can lead to unstable population oscillations, suggesting the potential difficulty in the coexistence of antagonism and mutualism. Mutualism-induced instability arises from the indirect positive effect of mutualism on the exploiter. Furthermore, for a three-species system with a stronger mutualistic interaction to persist stably, a weaker antagonistic interaction is required. Network studies of communities composed of one type of interaction may not capture the dynamics of natural communities.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Adler LS (2000) Alkaloid uptake increases fitness in a hemiparasitis plant via reduces herbivory and increasse pollination. Am Nat 156:92–99

    Article  PubMed  Google Scholar 

  • Adler LS, Bronstein JL (2004) Attracting antagonists: does floral nectar increase leaf herbivory? Ecology 85:1519–1526

    Article  Google Scholar 

  • Allesina S, Levine JM (2011) Stability criteria for complex ecosystems. Proc Natl Acad Sci USA 108:5638–5642

    Article  PubMed Central  PubMed  Google Scholar 

  • Allesina S, Tang S (2012) Stability criteria for complex ecosystems. Nature 483:205–208

    Article  PubMed  CAS  Google Scholar 

  • Bacher S, Friedli J (2002) Dynamics of mutualism in a multi-species context. Proc R Soc Lond B 269:1517–1522

    Article  Google Scholar 

  • Bascompte J (2009) Mutualistic networks. Front Ecol Environ 8:429–436

    Article  Google Scholar 

  • Bascompte J, Jordano P, Merián CJ, Olesen JM (2003) The nested assembly of plant-animal mutualistic networks. Proc Natl Acad Sci USA 100:9383–9387

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Boucher DH (1985) The Biology of mutualism: ecology and evolution. Oxford University Press, New York

    Google Scholar 

  • Bronstein JL, Wilson WG, Morris WF (2003) Ecological dynamics of mutualist/antagonist communities. Am Nat 162:1–20

    Article  Google Scholar 

  • Fontaine C, Guimarães PR Jr, Kéfi S, Loeuille N, Memmott J, van der Putten WH, van Veen FJF, Thébault E (2011) The ecological and evolutionary implications of merging different types of networks. Ecol Lett 14:1170–1181

    Article  PubMed  Google Scholar 

  • Goldberg DE, Barton AM (1992) Patterns and consequences of interspecific competition in natural communities: a review of field experiments with plants. Am Nat 139:771–801

    Article  Google Scholar 

  • Golinski MR (2006) A review of theoretical approaches for studying the effects of interactions between mutualists and nonmutualists on community stability. Bull Ecol Soc Am 87:37–44

    Article  Google Scholar 

  • Hairston NG, Smith FE, Slobodkin LB (1960) Community structure, population control, and competition. Am Nat 94:421–425

    Article  Google Scholar 

  • Herrera CM, Medrano M, Rey PJ, Sánchez-Lafuente AM, García MB, Guitián J, Manzaneda AJ (2002) Interaction of pollinators and herbivores on plant fitness suggests a pathway for correlated evolution of mutualism- and antagonism-related traits. Proc Natl Acad Sci USA 99:16823–16828

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Hoeksema JD, Bruna EM (2000) Pursuing the big questions about interspecific mutualism: a review of theoretical approaches. Oecologia 125:321–330

    Article  Google Scholar 

  • Holland JN, DeAngelis DL, Bronstein JL (2002) Population dynamics and mutualism; functional responses of benefits and costs. Am Nat 159:231–244

    Article  PubMed  Google Scholar 

  • Holland JN, Ness JH, Boyle AL, Bronstein JL (2005) Mutualisms as consumer–resource interactions. In: Barbosa P, Castellanos I (eds) Ecology of predator–prey interactions. Oxford University Press, New York, pp 17–33

    Google Scholar 

  • Huisman J, Weissing FJ (1999) Biodiversity of plankton by species oscillations and chaos. Nature 402:407–410

    Article  Google Scholar 

  • Irwin RE, Adler LS, Brody AK (2004) The dual role of floral traits: pollinator attraction and plant defense. Ecology 85:1503–1511

    Article  Google Scholar 

  • Jang SR (2002) Dynamics of herbivore-plant-pollinator models. J Math Biol 44:129–149

    Article  PubMed  CAS  Google Scholar 

  • Kondoh M (2003) Foraging adaptation and the relationship between food –web complexity and stability. Science 299:1388–1391

    Article  PubMed  CAS  Google Scholar 

  • Kondoh M (2008) Building trophic modules into a persistent food web. Proc Natl Acad Sci USA 105:16631–16635

    Article  PubMed Central  PubMed  Google Scholar 

  • Kooi B, Huijper LDJ, Kooijman SALM (2004) Consequences of symbiosis for food web dynamics. J Math Biol 49:227–271

    Article  PubMed  CAS  Google Scholar 

  • MacArthur R (1970) Species packing and competitive equilibrium for many species. Theor Popul Biol 1:1–11

    Article  PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Martinez ND, Williams RJ, Dunne JA (2006) Diversity, complexity, and persistence in large model ecosystems. In: Pascual M, Dunne JA (eds) Ecological networks: linking structure to dynamics in food webs. Oxford University Press, Oxford, pp 163–185

    Google Scholar 

  • May RM (1972) Will a large complex system be stable? Nature 238:413–414

    Article  PubMed  CAS  Google Scholar 

  • May RM (1974) Stability and complexity in model ecosystems. Princeton University Press, Princeton

    Google Scholar 

  • May RM (1981) Models of two interacting populations. In: May RM (ed) Theoretical ecology. Sinauer, Sunderland, pp 78–104

    Google Scholar 

  • McCann K, Hastings A, Huxel GR (1998) Weak trophic interactions and the balance of nature. Nature 395:794–798

    Article  CAS  Google Scholar 

  • Melián CJ, Bascompte J, Jordano P, Krivan V (2009) Diversity in a complex ecological network with two interaction types. Oikos 118:122–130

    Article  Google Scholar 

  • Morris WF, Bronstein JL, Wilson WG (2003) Three-way coexistence in obligate mutualist–exploiter interactions: the potential role for of competition. Am Nat 161:860–875

    Article  PubMed  Google Scholar 

  • Mougi A, Kondoh M (2012) Diversity of interaction types and ecological community stability. Science 337:349–351

    Article  PubMed  CAS  Google Scholar 

  • Murdoch W, Briggs C, Nisbet R (2003) Consumer-resource dynamics. Princeton University Press, Princeton

    Google Scholar 

  • Okuyama T, Holland JN (2008) Network structural properties mediate the stability of mutualistic communities. Ecol Lett 11:208–216

    Article  PubMed  Google Scholar 

  • Otto SB, Rall BC, Brose U (2007) Allometric degree distributions facilitate food-web stability. Nature 450:1226–1230

    Article  PubMed  CAS  Google Scholar 

  • Ringel MS, Hu HH, Anderson G (1996) The stability and persistence of mutualisms embedede in community interactions. Theor Popul Biol 50:281–297

    Article  PubMed  CAS  Google Scholar 

  • Rosenzweig ML (1971) Paradox of enrichment: destabilization of exploitation ecosystems in ecological time. Science 171:385–387

    Article  PubMed  CAS  Google Scholar 

  • Rozdilsky ID, Stone L (2001) Complexity can enhance stability in competitive systems. Ecol Lett 4:397–400

    Article  Google Scholar 

  • Schultz JC, Baldwin IT (1982) Oak leaf quality declines in response to defoliation by gypsy moth larvae. Science 217:149–151

    Article  PubMed  CAS  Google Scholar 

  • Smith DC, Douglas AE (1987) The biology of symbiosis. Edward Arnold, London

    Google Scholar 

  • Smith HL, Waltman P (1995) The theory of the chemostat. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Stouffer DB, Bascompte J (2009) Understanding food-web persistence from local to global scales. Ecol Lett 13:154–161

    Article  PubMed  Google Scholar 

  • Thompson JN (2005) The geographic mosaic of coevolution. University of Chicago Prss, Chicago

    Google Scholar 

  • Thompson AR, Nisbet RM, Schmitt RJ (2006) Dynamics of mutualist populations that are demographically open. J Anim Ecol 75:1239–1251

    Article  PubMed  Google Scholar 

  • Wilson WG, Morris WF, Bronstein JL (2003) Coexistence of mutualists and exploiters on spatial landscapes. Ecol Monogr 73:397–413

    Article  Google Scholar 

  • Wright DH (1989) A simple, stable model of mutualism incorporating handling time. Am Nat 134:664–667

    Article  Google Scholar 

Download references

Acknowledgments

This study was supported by the Environment Research and Technology Development Fund (D-1102) of the Ministry of the Environment, Japan, by a Grant-in-Aid for Scientific Research (B) (#20370009), by a Grant-in-Aid for Young Scientists (B) (#25840164), and by a Grant-in-Aid for Challenging Exploratory Research (#23657019) from the Japan Society for the Promotion of Science.

Author information

Authors and Affiliations

  1. Department of Biological Science, Faculty of Life and Environmental Science, Shimane University, 1060 Nishikawatsu-cho, Matsue, 690-8504, Japan

    Akihiko Mougi

  2. Department of Environmental Solution Technology, Faculty of Science and Technology, Ryukoku University, 1-5 Yokoya, Seta Oe-cho, Otsu, 520-2194, Japan

    Michio Kondoh

Authors
  1. Akihiko Mougi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Michio Kondoh
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Akihiko Mougi.

Additional information

Akihoko Mougi is the recipient of the 6th Population Ecology Young Scientist Award.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 290 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Mougi, A., Kondoh, M. Instability of a hybrid module of antagonistic and mutualistic interactions. Popul Ecol 56, 257–263 (2014). https://doi.org/10.1007/s10144-014-0430-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10144-014-0430-9

Keywords

Search

Navigation