A conceptual framework for studying the strength of plant-animal mutualistic interactions

Ecology Letters

Volumn 18, Issue 4, 2015, Pages 385-400

  Vázquez, Diego P ^a,b   Ramos Jiliberto, Rodrigo ^c,d   Urbani, Pasquinell ^c   Valdovinos, Fernanda S ^e,f  

^a Facultad de Ciencias Naturales e Instituto M Lillo   (Argentina)

^b UNIVERSIDAD NACIONAL DE CUYO   (Argentina)

^c UNIVERSITY OF CHILE   (Chile)

^d Instituto de Filosofía y Ciencias de la Complejidad IFICC Los Alerces 3024 Ñuñoa   (Chile)

^e University of Arizona   (United States)

^f Pacific Ecoinformatics and Computational Ecology Lab   (United States)

Author keywords

Ecological networks; Interaction strength; Long term effects; Mutualism; Plant animal interactions; Short term effects

Indexed keywords

ANIMAL COMMUNITY; CONCEPTUAL FRAMEWORK; DATA INTERPRETATION; FIELD SURVEY; FOOD WEB; LONG-TERM CHANGE; MUTUALISM; PLANT COMMUNITY;

ANIMALIA;

ANIMAL; BIOLOGICAL MODEL; ECOLOGY; FOOD CHAIN; PLANT; POPULATION DYNAMICS; PROCEDURES; STATISTICAL MODEL; SYMBIOSIS;

ANIMALS; ECOLOGY; FOOD CHAIN; LOGISTIC MODELS; MODELS, BIOLOGICAL; PLANTS; POPULATION DYNAMICS; SYMBIOSIS;

EID: 84925637774     PISSN: 1461023X     EISSN: 14610248     Source Type: Journal    
DOI: 10.1111/ele.12411     Document Type: Review

References (92)

1. Abrams, P.A. (1987). On classifying interactions between populations. Oecologia, 73, 272-281.
2. Abrams, P.A. (2001). Describing and quantifying interspecific interactions: a commentary on recent approaches. Oikos, 94, 209-218.
3. Addicott, J.F. (1981). Stability properties of two-species models of mutualism: simulation studies. Oecologia, 49, 42-49.
4. Amarasekare, P. (2004). Spatial dynamics of mutualistic interactions. J. Anim. Ecol., 73, 128-142.
5. Andrews, J.F. (1968). A mathematical model for the continuous culture of microorganisms utilizing inhibitory substrates. Biotechnol. Bioeng., 10, 707-723.
6. Armstrong, R.A. (1987). A patch model of mutualism. J. Theor. Biol., 125, 243-246.
7. ArunKumar, N. & Venkatesan, P. (2011). Recent advancement in causal inference. Int. J. Pharm. Sci. Rev. Res., 2, 10-19.
8. Ashman, T.L., Knight, T.M., Steets, J.A., Amarasekare, P., Burd, M., Campbell, D.R., Dudash, M.R., Johnston, M.O., Mazer, S.J., Mitchell, R.J., Morgan, M.T. & Wilson, W.G. (2004). Pollen limitation of plant reproduction: ecological and evolutionary causes and consequences. Ecology, 85, 2408-2421.
9. Bascompte, J., Jordano, P., Melián, C.J. & Olesen, J.M. (2003). The nested assembly of plant-animal mutualistic networks. Proc. Natl. Acad. Sci. USA, 100, 9383-9387.
10. Bascompte, J., Jordano, P. & Olesen, J.M. (2006). Asymmetric coevolutionary networks facilitate biodiversity maintenance. Science, 312, 431-433.
11. Bastolla, U., Fortuna, M.A., Pascual-Garcia, A., Ferrera, A., Luque, B. & Bascompte, J. (2009). The architecture of mutualistic networks minimizes competition and increases biodiversity. Nature, 458, 1018-1020.
12. Begon, M., Townsend, C.R. & Harper, J.L. (2006). Ecology: From Individuals to Ecosystems. Blackwell Publishing, Malden, MA, USA.
13. Bender, E.A., Case, T.J. & Gilpin, M.E. (1984). Perturbation experiments in community ecology: theory and practice. Ecology, 65, 1-13.
14. Berlow, E.L., Navarrete, S.A., Briggs, C.J., Power, M.E. & Menge, B.A. (1999). Quantifying variation in the strengths of species interactions. Ecology, 80, 2206-2224.
15. Berlow, E.L., Neutel, A.-M., Cohen, J.E., de Ruiter, P.C., Ebenman, B., Emmerson, M., et al. (2004). Interaction strengths in food webs: issues and opportunities. J. Anim. Ecol., 73, 585-598.
16. Bierzychudek, P. (1982). The demography of jack-in-the-pulpit, a forest perennial that changes sex. Ecol. Monogr., 52, 335-351.
17. Bronstein, J.L. (1994). Our current understanding of mutualism. Q. Rev. Biol., 69, 31-51.
18. Brose, U., Berlow, E.L. & Martinez, N.D. (2005). Scaling up keystone effects from simple to complex ecological networks. Ecol. Lett., 8, 1317-1325.
19. Brose, U., Ostling, A., Harrison, K. & Martinez, N.D. (2004). Unified spatial scaling of species and their trophic interactions. Nature, 428, 167-171.
20. Brosi, B.J. & Briggs, H.M. (2013). Single pollinator species losses reduce floral fidelity and plant reproductive function. Proc. Natl. Acad. Sci. USA, 110, 13044-13048.
21. Bruna, E.M., Fiske, I.J. & Trager, M.D. (2009). Habitat fragmentation and plant populations: is what we know demographically irrelevant? J. Veg. Sci., 20, 569-576.
22. Bruno, J.F., Stachowicz, J.J. & Bertness, M.D. (2003). Inclusion of facilitation into ecological theory. Trends Ecol. Evol., 18, 119-125.
23. Caswell, H. (2001). Matrix Population Models: Construction, Analysis, and Interpretation. Sinauer Associates, Suntherland, MA.
24. Crone, E.E. (2001). Is survivorship a better fitness surrogate than fecundity? Evolution, 55, 2611-2614.
25. Dambacher, J.M., Levins, R. & Rossignol, P.A. (2005). Life expectancy change in perturbed communities: derivation and qualitative analysis. Math. Biosci., 197, 1-14.
26. Dambacher, J.M. & Ramos-Jiliberto, R. (2007). Understanding and predicting effects of modified interactions through a qualitative analysis of community structure. Q. Rev. Biol., 82, 227-250.
27. Ehrlén, J. & Eriksson, O. (1995). Pollen limitation and population growth in a herbaceous perennial legume. Ecology, 76, 652-656.
28. Emmerson, M.C. & Raffaelli, D. (2004). Predator-prey body size, interaction strength and the stability of a real food web. J. Anim. Ecol., 73, 399-409.
29. Encinas-Viso, F., Revilla, T.A. & Etienne, R.S. (2012). Phenology drives mutualistic network structure and diversity. Ecol. Lett., 15, 198-208.
30. Feldman, T.S. & Morris, W.F. (2011). Higher survival at low density counteracts lower fecundity to obviate allee effects in a perennial plant. Afr. J. Ecol., 99, 1162-1170.
31. Fleming, T.H. & Williams, C.F. (1990). Phenology, seed dispersal, and recruitment in cecropia peltata (moraceae) in costa rican tropical dry forest. J. Trop. Ecol., 6, 163-178.
32. Fortuna, M.A. & Bascompte, J. (2006). Habitat loss and the structure of plant-animal mutualistic networks. Ecol. Lett., 9, 281-286.
33. Garibaldi, L.A., Steffan-Dewenter, I., Winfree, R., Aizen, M.A., Bommarco, R., Cunningham, S.A., et al. (2013). Wild pollinators enhance fruit set of crops regardless of honey bee abundance. Science, 339, 1608-1611.
34. Gause, G.F. & Witt, A.A. (1935). Behavior of mixed populations and the problem of natural selection. Am. Nat., 69, 596-609.
35. Heithaus, E.R., Culver, D.C. & Beattie, A.J. (1980). Models of ant-plant mutualisms. Am. Nat., 116, 347.
36. Herrera, C.M. (1987). Components of pollinator quality: comparative analysis of a diverse insect assemblage. Oikos, 50, 79-90.
37. Herrera, C.M. (1989). Pollinator abundance, morphology, and flower visitation rate: analysis of the quantity component in a plant-pollinator system. Oecologia, 80, 241-248.
38. Holland, J.N. & DeAngelis, D.L. (2010). A consumer-resource approach to the density-dependent population dynamics of mutualism. Ecology, 91, 1286-1295.
39. Holland, J.N., DeAngelis, D.L. & Bronstein, J.L. (2002). Population dynamics and mutualism: functional responses of benefits and costs. Am. Nat., 159, 231-244.
40. Holland, J.N., Okuyama, T. & DeAngelis, D.L. (2006). Comment on 'asymmetric coevolutionary networks facilitate biodiversity maintenance'. Science, 313, 1887.
41. Jordano, P. & Schupp, E.W. (2000). Seed disperser effectiveness: the quantity component and patterns of seed rain for prunus mahaleb. Ecol. Monogr., 70, 591-615.
42. Knight, T.M. (2004). The effects of herbivory and pollen limitation on a declining population of trillium grandiflorum. Ecol. Appl., 14, 915-928.
43. Laska, M.S. & Wooton, J.T. (1998). Theoretical concepts and empirical approaches to measuring interaction strength. Ecology, 79, 461-476.
44. Law, W., Salick, J. & Knight, T.M. (2010). The effects of pollen limitation on population dynamics of snow lotus (Saussurea medusa and S. laniceps, asteraceae): Threatened Tibetan medicinal plants of the eastern Himalayas. Plant Ecol., 201, 343-357.
45. Levins, R. (1968). Evolution in Changing Environments. Princeton University Press, Princeton, NJ.
46. Levitan, C. (1987). Formal stability analysis of a planktonic freshwater community. In: Predation: Direct and Indirect Impacts on Aquatic Communities (eds Kerfoot, W.C. & Sih, A.). University Press of New England, Hanover, pp. 71-100.
47. Lopezaraiza-Mikel, M., Hayes, R., Whalley, M. & Memmott, J. (2007). The impact of an alien plant on a native plant-pollinator network: an experimental approach. Ecol. Lett., 10, 539-550.
48. MacArthur, R.H. (1972). Geographical Ecology. Princeton University Press, Princeton, NJ.
49. May, R.M. (1973). Stability and Complexity in Model Ecosystems, 1st edn. Princeton University Press, Princeton, NJ.
50. May, R.M. (1976). Mathematical aspects of the dynamics of animal populations. In: Studies in Mathematical Biology (ed. Levin, S.A.). American Mathematical Society, Providence, pp. 317-366.
51. May, R.M. (1981). Models for two interacting populations. In: Theoretical Ecology: Principles and Applications (ed. May, R.M.). Blackwell Scientific, Oxford, UK, pp. 49-70.
52. McCann, K., Hastings, A. & Huxel, G.R. (1998). Weak trophic interactions and the balance of nature. Nature, 395, 794-797.
53. Morris, W.F., Vázquez, D.P. & Chacoff, N.P. (2010). Benefit and cost curves for typical pollination mutualisms. Ecology, 91, 1276-1285.
54. Nakazawa, T. & Doi, H. (2012). A perspective on match/mismatch of phenology in community contexts. Oikos, 121, 489-495.
55. Ness, J.H., Morris, W.F. & Bronstein, J.L. (2006). Integrating quality and quantity of mutualistic service to contrast ant species protecting Ferocactus wislizeni. Ecology, 87, 912-921.
56. Novak, M. (2010). Estimating interaction strengths in nature: experimental support for an observational approach. Ecology, 91, 2394-2405.
57. Novak, M. & Wootton, J. (2008). Estimating nonlinear interaction strengths: an observation-based method for species-rich food webs. Ecology, 89, 2083-2089.
58. Okuyama, T. & Holland, J.N. (2008). Network structural properties mediate the stability of mutualistic communities. Ecol. Lett., 11, 208-216.
59. Olsen, K.M. (1997). Pollination effectiveness and pollinator importance in a population of heterotheca subaxillaris (asteraceae). Oecologia, 109, 114-121.
60. Paine, R.T. (1980). Food webs: linkage, interaction strength and community infrastructure. J. Anim. Ecol., 49, 667-685.
61. Paine, R.T. (1992). Food-web analysis through field measurement of per capita interaction strength. Nature, 355, 73-75.
62. Parker, I.M. (1997). Pollinator limitation of Cytisus scoparius (scotch broom), an invasive exotic shrub. Ecology, 78, 1457-1470.
63. Pascual, M.A. & Kareiva, P. (1996). Predicting the outcome of competition using experimental data: maximum likelihood and bayesian approaches. Ecology, 77, 337-349.
64. Pearl, J. (2009). Causal inference in statistics: an overview. Stat. Surv., 3, 96-146.
65. Pettersson, M.W. (1991). Pollination by a guild of fluctuating moth populations: option for unspecialization in silence vulgaris. Afr. J. Ecol., 79, 591-604.
66. Ramos-Jiliberto, R., Albornoz, A.A., Valdovinos, F.S., Smith-Ramìrez, C., Arim, M., Armesto, J.J., et al. (2009). A network analysis of plant-pollinator interactions in temperate rain forests of chiloé island, chile. Oecologia, 160, 697-706.
67. Ramos-Jiliberto, R., Valdovinos, F.S., Moisset de Espanés, P. & Flores, J.D. (2012). Topological plasticity incaeses robustness of mutualistic networks. J. Anim. Ecol., 81, 896-904.
68. Reed, D.H. & Bryant, E.H. (2004). Phenotypic correlations among fitness and its components in a population of the housefly. J. Evol. Biol., 17, 919-923.
69. Ringel, M.S., Hu, H.H. & Anderson, G. (1996). The stability and persistence of mutualisms embedded in community interactions. Theor. Popul. Biol., 50, 281-297.
70. Roulston, T.H. & Goodell, K. (2011). The role of resources and risks in regulating wild bee populations. Annu. Rev. Entomol., 56, 293-312.
71. Sahli, H. & Conner, J. (2006). Characterizing ecological generalization in plant-pollination systems. Oecologia, 148, 365-372.
72. Sala, E. & Graham, M.H. (2002). Community-wide distribution of predator-prey interaction strength in kelp forests. Proc. Natl. Acad. Sci. USA, 99, 3678-3683.
73. Schemske, D.W. & Horvitz, C.C. (1984). Variation among floral visitors in pollination ability: a precondition for mutualism specialization. Science, 225, 519-521.
74. Schmitz, O.J. (1997). Press perturbations and the predictability of ecological interactions in a food web. Ecology, 78, 55-69.
75. Schupp, E.W. (1993). Quantity, quality, and the effectiveness of seed dispersal by animals. In: Frugivory and Seed Dispersal: Ecological and Evolutionary Aspects (eds Fleming, T.H. & Estrada, A.). Kluwer Academic Publishers, Dordrecht, 15-29.
76. Schupp, E.W., Jordano, P. & Gómez, J.M. (2010). Seed dispersal effectiveness revisited: a conceptual review. New Phytol., 188, 333-353.
77. Stachowicz, J.J. (2001). Mutualism, facilitation, and the structure of ecological communities. Bioscience, 51, 235-246.
78. Travis, C.C. & Post, W.M. (1979). Dynamics and comparative statics of mutualistic communities. J. Theor. Biol., 78, 553-571.
79. Valdovinos, F.S., Moisset de Espanés, P., Flores, J.D. & Ramos-Jiliberto, R. (2013). Adaptive foraging allows the maintenance of biodiversity of pollination networks. Oikos, 122, 907-917.
80. Valdovinos, F.S., Ramos-Jiliberto, R., Flores, J.D., Espinoza, C. & López, G. (2009). Structure and dynamics of pollination networks: the role of alien plants. Oikos, 118, 1190-1200.
81. Vandermeer, J.H. & Boucher, D.H. (1978). Varieties of mutualistic interactions in population models. J. Theor. Biol., 74, 549-558.
82. Vázquez, D.P., Lomáscolo, S.B., Maldonado, M.B., Chacoff, N.P., Dorado, J., Stevani, E.L., et al. (2012). The strength of plant-pollinator interactions. Ecology, 93, 719-725.
83. Vázquez, D.P., Morris, W.F. & Jordano, P. (2005). Interaction frequency as a surrogate for the total effect of animal mutualists on plants. Ecol. Lett., 8, 1088-1094.
84. Wheelwright, N.T. (1991). How long do fruit-eating birds stay in the plants where they feed. Biotropica, 23, 29-40.
85. Whittaker, R.H. (1975). Communities and Ecosystems. MacMillan, New York.
86. Wolin, C.L. & Lawlor, L.R. (1984). Models of facultative mutualism: density effects. Am. Nat., 124, 843-862.
87. Woodward, G., Ebenman, B., Emmerson, M., Montoya, J., Olesen, J., Valido, A., et al. (2005). Body size in ecological networks. Trends Ecol. Evol., 20, 402-409.
88. Wootton, J.T. (1997). Estimates and tests of per capita interaction strength: diet, abundance, and impact of intertidally foraging birds. Ecol. Monogr., 67, 45-64.
89. Wootton, J.T. & Emmerson, M. (2005). Measurement of interaction strength in nature. Annu. Rev. Ecol. Evol. Syst., 36, 419-444.
90. Yodzis, P. (1981). The stability of real ecosystems. Nature, 289, 674-676.
91. Yodzis, P. (1988). The indeterminacy of ecological interactions as perceived through perturbation experiments. Ecology, 69, 508-515.
92. Yodzis, P. & Innes, S. (1992). Body size and consumer-resource dynamics. Am. Nat., 139, 1151-1175.