Advertisement

Theoretical Ecology

, Volume 6, Issue 4, pp 475–493 | Cite as

Consumer–resource dynamics of indirect interactions in a mutualism–parasitism food web module

  • J. Nathaniel HollandEmail author
  • Yuanshi Wang
  • Shan Sun
  • Donald L. DeAngelis
Original Paper

Abstract

Food web dynamics are well known to vary with indirect interactions, classic examples including apparent competition, intraguild predation, exploitative competition, and trophic cascades of food chains. Such food web modules entailing predation and competition have been the focus of much theory, whereas modules involving mutualism have received far less attention. We examined an empirically common food web module involving mutualistic (N 2) and parasitic (N 3) consumers exploiting a resource of a basal mutualist (N 1), as illustrated by plants, pollinators, and nectar robbers. This mutualism–parasitism food web module is structurally similar to exploitative competition, suggesting that the module of two consumers exploiting a resource is unstable. Rather than parasitic consumers destabilizing the module through (−,−) indirect interactions, two mechanisms associated with the mutualism can actually enhance the persistence of the module. First, the positive feedback of mutualism favors coexistence in stable limit cycles, whereby (+,−) indirect interactions emerge in which increases in N 2 have positive effects on N 3 and increases in N 3 have negative effects on N 2. This (+,−) indirect interaction arising from the saturating positive feedback of mutualism has broad feasibility across many types of food web modules entailing mutualism. Second, optimization of resource exploitation by the mutualistic consumer can lead to persistence of the food web module in a stable equilibrium. The mutualism–parasitism food web module is a basic unit of food webs in which mutualism favors its persistence simply through density-dependent population dynamics, rather than parasitism destabilizing the module.

Keywords

Community Interaction strength Model Mutualism Parasitism Plant–pollinator–nectar robber 

Notes

Acknowledgments

We thank W.F. Morris, S. Schreiber, and the anonymous reviewers for their comments which have improved this study. S.S. acknowledges support by the National Natural Science Foundation of China grant no. 31100277 and the Fundamental Research Funds for the Central Universities (lzujbky-2013-99). Y.W. acknowledges the support by NSKF of China grant no. 60736028, NSFC grant no. 11171355, and NSF of Guangdong Province S2012010010320. D.L.D. was supported by the US Geological Survey’s Southeastern Ecological Science Center. J.N.H. and D.L.D. acknowledge the support from NSF grants DEB-0814523 and DEB-1147630.

References

  1. Abrams PA, Ginzburg LR (2000) The nature of predation: prey dependent, ratio dependent or neither? Trends Ecol Evol 15:337–341PubMedCrossRefGoogle Scholar
  2. Agrawal AA, Ackerly DD, Adler F, Arnold AE, Cáceres C, Doak DF, Post E, Hudson PJ, Maron J, Mooney KA, Power M, Schemske DW, Stachowicz J, Strauss SY, Turner MG, Werner E (2007) Filling key gaps in population and community ecology. Front Ecol Environ 5:145–152CrossRefGoogle Scholar
  3. Allesina S, Pascual M (2008) Network structure, predator–prey modules, and stability in large food webs. Theor Ecol 1:55–64CrossRefGoogle Scholar
  4. Allesina S, Tang S (2012) Stability criteria for complex ecosystems. Nature 483:205–208PubMedCrossRefGoogle Scholar
  5. Armstrong RA, McGehee R (1976) Coexistence of species competing for shared resources. Theoretical Population Dynamics 9:317–328CrossRefGoogle Scholar
  6. Axelrod R, Hamilton WD (1981) The evolution of cooperation. Science 211:1390–1396PubMedCrossRefGoogle Scholar
  7. Bascompte J, Melian CJ (2005) Simple trophic modules for complex food webs. Ecology 86:2868–2873CrossRefGoogle Scholar
  8. Bascompte J, Jordano P (2007) Plant–animal mutualistic networks: the architecture of biodiversity. Annu Rev Ecol Evol Syst 38:567–593CrossRefGoogle Scholar
  9. Bascompte J, Jordano P, Melianand CJ, Olesen JM (2003) The nested assembly of plant–animal mutualistic networks. Proc Natl Acad Sci USA 100:9383–9387PubMedCrossRefGoogle Scholar
  10. Beddington JR (1975) Mutual interference between parasites or predators and its effect on searching efficiency. J Anim Ecol 44:331–430CrossRefGoogle Scholar
  11. Bronstein JL (2001) The exploitation of mutualisms. Ecol Lett 4:277–287CrossRefGoogle Scholar
  12. Bronstein JL, Wilson WG, Morris WF (2003) Ecological dynamics of mutualist/antagonist communities. Am Nat 162:S24–S39PubMedCrossRefGoogle Scholar
  13. Bull JJ, Rice WR (1991) Distinguishing mechanisms for the evolution of cooperation. J Theor Biol 149:63–74PubMedCrossRefGoogle Scholar
  14. Chesson P (2000) Mechanisms of maintenance of species diversity. Annu Rev Ecol Syst 31:343–366CrossRefGoogle Scholar
  15. Crowley PH, Cox JJ (2011) Intraguild mutualism. Trends Ecol Evol 26:627–633PubMedCrossRefGoogle Scholar
  16. DeAngelis DL, Goldstein RA, O’Neill RV (1975) A model for trophic interaction. Ecology 56:881–892CrossRefGoogle Scholar
  17. Doebeli M, Knowlton N (1998) The evolution of interspecific mutualism. Proc Natl Acad Sci USA 95:8676–8680PubMedCrossRefGoogle Scholar
  18. Ferriere R, Bronstein JL, Rinaldi S, Law R, Gauduchon M (2002) Cheating and the evolutionary stability of mutualisms. Proc R Soc Lond B 269:773–780CrossRefGoogle Scholar
  19. Fishman MA, Hadany L (2010) Plant–pollinator population dynamics. Theor Popul Biol 78:270–277PubMedCrossRefGoogle Scholar
  20. Fontaine C, Guimaraes PR Jr, Kefi S, Loeuille N, Memmott J, van der Putten WH, van Veen FJF, Thebault E (2011) The ecological and evolutionary implications of merging different types of networks. Ecol Lett 14:1170–1181PubMedCrossRefGoogle Scholar
  21. Foster KR, Kokko H (2006) Cheating can stabilize cooperation in mutualisms. Proc R Soc Biol Sci B 273:2233–2239CrossRefGoogle Scholar
  22. Genini J, Morellato LPC, Guimaraes PR Jr, Olesen JM (2010) Cheaters in mutualism networks. Biol Lett 6:494–497PubMedCrossRefGoogle Scholar
  23. Goudard A, Loreau M (2008) Nontrophic interactions, biodiversity, and ecosystem functioning: an interaction web model. Am Nat 171:91–106PubMedCrossRefGoogle Scholar
  24. Hairston NG, Smith FE, Slobodkin LB (1960) Community structure, population control, and competition. Am Nat 94:421–425CrossRefGoogle Scholar
  25. Holland JN, DeAngelis DL (2009) Consumer–resource theory predicts dynamic transitions between outcomes of interspecific interactions. Ecol Lett 12:1357–1366PubMedCrossRefGoogle Scholar
  26. Holland JN, DeAngelis DL (2010) A consumer–resource approach to the density-dependent population dynamics of mutualism. Ecology 91:1286–1295PubMedCrossRefGoogle Scholar
  27. Holt RD (1977) Predation, apparent competition, and the structure of prey communities. Theor Popul Biol 12:197–229PubMedCrossRefGoogle Scholar
  28. Holt RD, Grover J, Tilman D (1994) Simple rules for interspecific dominance in systems with exploitative and apparent competition. Am Nat 144:741–771CrossRefGoogle Scholar
  29. Holt RD, Polis GA (1997) A theoretical framework for intraguild predation. Am Nat 149:745–764CrossRefGoogle Scholar
  30. Hsu SB, Hubbell SP, Waltman P (1978) A contribution to the theory of competing predators. Ecol Monogr 48:337–349CrossRefGoogle Scholar
  31. Ings TC, Montoya JM, Bascompte J, Bluethgen N, Brown L, Dormann CF, Edwards F, Figueroa D, Jacob U, Jones JI, Lauridsen RB, Ledger ME, Lewis HM, Olesen JM, Frank van Veen FJ, Warren PH, Woodward G (2009) Ecological networks—beyond food webs. J Anim Ecol 78:253–269PubMedCrossRefGoogle Scholar
  32. Irwin RE, Bronstein JL, Manson JS, Richardson L (2010) Nectar robbing: ecological and evolutionary perspectives. Annu Rev Ecol Evol Syst 41:271–292CrossRefGoogle Scholar
  33. Jones EI, Ferriere R, Bronstein JL (2009) Eco-evolutionary dynamics of mutualists and exploiters. Am Nat 174:780–794PubMedCrossRefGoogle Scholar
  34. Jordano P (1987) Patterns of mutualistic interactions in pollination and seed dispersal—connectance, dependence asymmetries and coevolution. Am Nat 129:657–677CrossRefGoogle Scholar
  35. Jordano P, Bascompte J, Olesen JM (2003) Invariant properties in eco-evolutionary networks of plant–animal interactions. Ecol Lett 6:69–81CrossRefGoogle Scholar
  36. Katrina P, Vos M, Bateman A, Anholt BR (2009) Functional responses modified by predator density. Oecologia 159:425–433CrossRefGoogle Scholar
  37. Kawanabe H, Cohen JE, Iwasaki K (1993) Mutualism and community organization: behavioural, theoretical, and food-web approaches. Oxford University Press, OxfordGoogle Scholar
  38. Kefi S, Berlow E, Wieters E, Navarrete S, Petchey O, Wood S, Boit A, Joppa L, Lafferty K, Williams R, Martinez N, Menge B, Blanchette C, Iles A, Brose U (2012) More than a meal… Integrating non-feeding interactions into food webs. Ecol Lett 15:291–300CrossRefGoogle Scholar
  39. Knight TM, McCoy MW, Chase JM, McCoy KA, Holt RD (2005) Trophic cascades across ecosystems. Nature 437:880–883PubMedCrossRefGoogle Scholar
  40. Knight TM, Chase JM, Hillebrand H, Holt RD (2006) Predation on mutualists can reduce the strength of trophic cascades. Ecol Lett 9:1173–1178PubMedCrossRefGoogle Scholar
  41. Kondoh M (2008) Building trophic modules into a persistent food web. Proc Natl Acad Sci of the USA 105:16631–16635CrossRefGoogle Scholar
  42. Law R, Bronstein JL, Ferriere R (2001) On mutualists and exploiters: plant–insect coevolution in pollinating seed–parasite systems. J Theor Biol 212:373–389PubMedCrossRefGoogle Scholar
  43. Lee CT, Inouye BD (2010) Mutualism between consumers and their shared resource can promote coexistence. Am Nat 175:277–288PubMedCrossRefGoogle Scholar
  44. Leon JA, Tumpson DB (1975) Competition between two species for two complementary or substitutable resources. J Theor Biol 50:185–201PubMedCrossRefGoogle Scholar
  45. Levine SH (1976) Competitive interactions in ecosystems. Am Nat 110:903–910CrossRefGoogle Scholar
  46. May RM (1974) Stability and complexity in model ecosystems. Princeton University Press, PrincetonGoogle Scholar
  47. McCann KS (2012) Food webs. Princeton University Press, PrincetonGoogle Scholar
  48. Menge BA (1995) Indirect effects in marine rocky intertidal interaction webs: patterns and importance. Ecol Monogr 65:21–74CrossRefGoogle Scholar
  49. Morris WF, Bronstein JL, Wilson WG (2003) Three-way coexistence in obligate mutualist–exploiter interactions: the potential role of competition. Am Nat 161:860–875PubMedCrossRefGoogle Scholar
  50. Odum EP, Biever LJ (1984) Resource quality, mutualism, and energy partitioning in food webs. Am Nat 124:360–376CrossRefGoogle Scholar
  51. Oksanen L, Fretwell SD, Arruda J, Niemela P (1981) Exploitation ecosystems in gradients of primary productivity. Am Nat 118:240–261CrossRefGoogle Scholar
  52. Oksanen L (1988) Ecosystem organization: mutualism and cybernetics or plain Darwinian struggle for existence. Am Nat 131:424–444CrossRefGoogle Scholar
  53. Okuyama T, Holland JN (2008) Network structural properties mediate the stability of mutualistic communities. Ecol Lett 11:208–216PubMedCrossRefGoogle Scholar
  54. Paine RT (1980) Food webs: linkage, interaction strength, and community infrastructure. J Anim Ecol 49:667–685CrossRefGoogle Scholar
  55. Peacor SD, Werner EE (2004) How dependent are species pair interaction strengths on other species in the food web? Ecology 85:2754–2763CrossRefGoogle Scholar
  56. Pimm SL (1982) Food webs. University of Chicago Press, ChicagoCrossRefGoogle Scholar
  57. Pires MM, Prado PI, Guimaraes PR (2011) Do food web models reproduce the structure of mutualistic networks? PLoS One 6:e27280PubMedCrossRefGoogle Scholar
  58. Polis GA, Strong DR (1996) Food web complexity and community dynamics. Am Nat 147:813–846CrossRefGoogle Scholar
  59. Polis GA, Winemiller KO (1996) Food webs: integration of patterns and dynamics. Chapman and Hall, New YorkGoogle Scholar
  60. Ringel MS, Hu HH, Anderson G (1996) The stability and persistence of mutualisms embedded in community interactions. Theor Popul Biol 50:281–297PubMedCrossRefGoogle Scholar
  61. Rosenzweig ML (1969) Why the prey curve has a hump. Am Nat 103:81–87CrossRefGoogle Scholar
  62. Rosenzweig ML (1971) Paradox of enrichment: destabilization of exploitation ecosystems in ecological time. Science 171:385–387PubMedCrossRefGoogle Scholar
  63. Rosenzweig ML, MacArthur RH (1963) Graphical representation and stability conditions of predator–prey systems. Am Nat 97:209–223CrossRefGoogle Scholar
  64. Skalski GT, Gilliam JF (2001) Functional responses with predator interference: viable alternatives to the Holling Type II model. Ecology 82:3083–3092CrossRefGoogle Scholar
  65. Stanton ML (2003) Interacting guilds: moving beyond the pairwise perspective on mutualisms. Am Nat 162:S10–S23PubMedCrossRefGoogle Scholar
  66. Stone L, Roberts A (1991) Conditions for a species to gain advantage from the presence of competitors. Ecology 72:1964–1972CrossRefGoogle Scholar
  67. Stouffer DB, Bascompte J (2010) Understanding food web persistence from local to global scales. Ecol Lett 13:154–161PubMedCrossRefGoogle Scholar
  68. Thebault E, Fontaine C (2010) Stability of ecological communities and the architecture of mutualistic and trophic networks. Science 329:853–856PubMedCrossRefGoogle Scholar
  69. Tilman D (1982) Resource competition and community structure. Princeton University Press, PrincetonGoogle Scholar
  70. Vandermeer J (1980) Indirect mutualism: variations on a theme by Stephen Levine. Am Nat 116:441–448CrossRefGoogle Scholar
  71. Vázquez DP, Blüthgen N, Cagnolo L, Chacoff NP (2009) Uniting pattern and process in plant–animal mutualistic networks: a review. Ann Bot 103:1445–1457PubMedCrossRefGoogle Scholar
  72. Werner EE, Peacor SD (2003) A review of trait-mediated indirect interactions in ecological communities. Ecology 84:1083–1100CrossRefGoogle Scholar
  73. Williams RJ (2008) Effects of network and dynamical model structure on species persistence in large model food webs. Theor Ecol 1:141–151CrossRefGoogle Scholar
  74. Wilson WG, Morris WF, Bronstein JL (2003) Coexistence of mutualists and exploiters on spatial landscapes. Ecol Monogr 73:397–413CrossRefGoogle Scholar
  75. Wootton JT (1994) The nature and consequences of indirect effects in ecological communities. Annu Rev Ecol Syst 25:443–466CrossRefGoogle Scholar
  76. Yu DW (2001) Parasites of mutualisms. Biol J Linn Soc 72:529–546CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  • J. Nathaniel Holland
    • 1
    Email author
  • Yuanshi Wang
    • 2
  • Shan Sun
    • 3
  • Donald L. DeAngelis
    • 4
  1. 1.Department of Biology and BiochemistryUniversity of HoustonHoustonUSA
  2. 2.School of Mathematics and Computational ScienceSun Yat-sen UniversityGuangzhouPeople’s Republic of China
  3. 3.Institute of Ecology, School of Life ScienceLanzhou UniversityLanzhouPeople’s Republic of China
  4. 4.US Geological Survey, Southeast Ecological Science Center, Department of BiologyUniversity of MiamiCoral GablesUSA

Personalised recommendations