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

The strength of species interactions influences strongly the structure and dynamics of ecological systems. Thus, quantifying such strength is crucial to understand how species interactions shape communities and ecosystems. Although the concepts and measurement of interaction strength in food webs have received much attention, there has been comparatively little progress in the context of mutualism. We propose a conceptual scheme for studying the strength of plant-animal mutualistic interactions. We first review the interaction strength concepts developed for food webs, and explore how these concepts have been applied to mutualistic interactions. We then outline and explain a conceptual framework for defining ecological effects in plant-animal mutualisms. We give recommendations for measuring interaction strength from data collected in field studies based on a proposed approach for the assessment of interaction strength in plant-animal mutualisms. This approach is conceptually integrative and methodologically feasible, as it focuses on two key variables usually measured in field studies: the frequency of interactions and the fitness components influenced by the interactions.

[1]  Oswald J. Schmitz,et al.  PRESS PERTURBATIONS AND THE PREDICTABILITY OFECOLOGICAL INTERACTIONS IN A FOOD WEB , 1997 .

[2]  R. Paine Food webs : linkage, interaction strength and community infrastructure , 1980 .

[3]  Donald L DeAngelis,et al.  Comment on "Asymmetric Coevolutionary Networks Facilitate Biodiversity Maintenance" , 2006, Science.

[4]  Jordi Bascompte,et al.  Asymmetric Coevolutionary Networks Facilitate Biodiversity Maintenance , 2006, Science.

[5]  D. H. Reed,et al.  Phenotypic correlations among fitness and its components in a population of the housefly , 2004, Journal of evolutionary biology.

[6]  M. Emmerson,et al.  MEASUREMENT OF INTERACTION STRENGTH IN NATURE , 2005 .

[7]  J. Wootton,et al.  ESTIMATES AND TESTS OF PER CAPITA INTERACTION STRENGTH: DIET, ABUNDANCE, AND IMPACT OF INTERTIDALLY FORAGING BIRDS , 1997 .

[8]  K. Olsen Pollination effectiveness and pollinator importance in a population of Heterotheca subaxillaris (Asteraceae) , 1996, Oecologia.

[9]  C. Herrera Components of pollinator "quality": comparative analysis of a diverse insect assemblage , 1987 .

[10]  N. T. Wheelwright How Long do Fruit-eating Birds Stay in the Plants Where They Feed?' , 1991 .

[11]  R. Levins Evolution in Changing Environments , 1968 .

[12]  Paulette Bierzychudek,et al.  The Demography of Jack‐in‐the‐Pulpit, a Forest Perennial that Changes Sex , 1982 .

[13]  Pablo A. Marquet,et al.  A network analysis of plant–pollinator interactions in temperate rain forests of Chiloé Island, Chile , 2009, Oecologia.

[14]  Jordi Bascompte,et al.  The architecture of mutualistic networks minimizes competition and increases biodiversity , 2009, Nature.

[15]  D. Vázquez,et al.  The strength of plant-pollinator interactions. , 2012, Ecology.

[16]  P. Yodzis The Indeterminacy of Ecological Interactions as Perceived Through Perturbation Experiments , 1988 .

[17]  P. Yodzis,et al.  The stability of real ecosystems , 1981, Nature.

[18]  E. Sala,et al.  Community-wide distribution of predator–prey interaction strength in kelp forests , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[19]  Peter Kareiva,et al.  Predicting the outcome of competition using experimental data : Maximum likelihood and bayesian approaches , 1996 .

[20]  M S Ringel,et al.  The stability and persistence of mutualisms embedded in community interactions. , 1996, Theoretical population biology.

[21]  E. Schupp Quantity, quality and the effectiveness of seed dispersal by animals , 1993, Vegetatio.

[22]  I. Parker POLLINATOR LIMITATION OF CYTISUS SCOPARIUS (SCOTCH BROOM), AN INVASIVE EXOTIC SHRUB , 1997 .

[23]  H. Caswell Matrix population models : construction, analysis, and interpretation , 2001 .

[24]  Ian J. Fiske,et al.  Habitat fragmentation and plant populations: is what we know demographically irrelevant? , 2009 .

[25]  J. Pearl Causal inference in statistics: An overview , 2009 .

[26]  H. Doi,et al.  A perspective on match/mismatch of phenology in community contexts , 2012 .

[27]  Judith L Bronstein,et al.  Population Dynamics and Mutualism: Functional Responses of Benefits and Costs , 2002, The American Naturalist.

[28]  R. Armstrong A patch model of mutualism , 1987 .

[29]  Mark Novak,et al.  Estimating interaction strengths in nature: experimental support for an observational approach. , 2010, Ecology.

[30]  I. Hiscock Communities and Ecosystems , 1970, The Yale Journal of Biology and Medicine.

[31]  E. Crone IS SURVIVORSHIP A BETTER FITNESS SURROGATE THAN FECUNDITY? , 2001, Evolution; international journal of organic evolution.

[32]  Priyanga Amarasekare,et al.  Spatial dynamics of mutualistic interactions , 2004 .

[33]  J. Stachowicz Mutualism, Facilitation, and the Structure of Ecological Communities , 2001 .

[34]  E. Berlow,et al.  QUANTIFYING VARIATION IN THE STRENGTHS OF SPECIES INTERACTIONS , 1999 .

[35]  R. Levins Evolution in Changing Environments: Some Theoretical Explorations. (MPB-2) , 1968 .

[36]  W. Morris,et al.  Integrating quality and quantity of mutualistic service to contrast ant species protecting Ferocactus wislizeni. , 2006, Ecology.

[37]  L. Lawlor,et al.  Models of Facultative Mutualism: Density Effects , 1984, The American Naturalist.

[38]  C. Herrera,et al.  Pollinator abundance, morphology, and flower visitation rate: analysis of the “quantity” component in a plant-pollinator system , 1989, Oecologia.

[39]  John F. Andrews,et al.  A mathematical model for the continuous culture of microorganisms utilizing inhibitory substrates , 1968 .

[40]  Pedro Jordano,et al.  Interaction frequency as a surrogate for the total effect of animal mutualists on plants , 2005 .

[41]  Rodrigo Ramos-Jiliberto,et al.  Adaptive foraging allows the maintenance of biodiversity of pollination networks , 2013 .

[42]  Peter A. Abrams,et al.  Describing and quantifying interspecific interactions: a commentary on recent approaches , 2001 .

[43]  W. Morris,et al.  Higher survival at low density counteracts lower fecundity to obviate Allee effects in a perennial plant , 2011 .

[44]  Michele R. Dudash,et al.  Pollen limitation of plant reproduction: Ecological and evolutionary causes and consequences , 2004 .

[45]  H. Briggs,et al.  Single pollinator species losses reduce floral fidelity and plant reproductive function , 2013, Proceedings of the National Academy of Sciences.

[46]  Jordi Bascompte,et al.  Habitat loss and the structure of plant-animal mutualistic networks. , 2006, Ecology letters.

[47]  Neo D. Martinez,et al.  Scaling up keystone effects from simple to complex ecological networks , 2005 .

[48]  T. Fleming,et al.  Phenology, seed dispersal, and recruitment in Cecropia peltata (Moraceae) in Costa Rican tropical dry forest , 1990, Journal of Tropical Ecology.

[49]  Rodrigo Ramos-Jiliberto,et al.  Structure and dynamics of pollination networks: the role of alien plants , 2009 .

[50]  David C. Culver,et al.  Models of Some Ant-Plant Mutualisms , 1980, The American Naturalist.

[51]  G. F. Gause,et al.  Behavior of Mixed Populations and the Problem of Natural Selection , 1935, The American Naturalist.

[52]  J. Bruno,et al.  Inclusion of facilitation into ecological theory , 2003 .

[53]  J. Vandermeer,et al.  Varieties of mutualistic interaction in population models. , 1978, Journal of theoretical biology.

[54]  D. Vázquez,et al.  Evaluating sampling completeness in a desert plant-pollinator network. , 2012, The Journal of animal ecology.

[55]  O. Eriksson,et al.  Pollen Limitation and Population Growth in a Herbaceous Perennial Legume , 1995 .

[56]  W. M. Post,et al.  Dynamics and comparative statics of mutualistic communities. , 1979, Journal of theoretical biology.

[57]  Annette Ostling,et al.  Unified spatial scaling of species and their trophic interactions , 2004, Nature.

[58]  K. Goodell,et al.  The role of resources and risks in regulating wild bee populations. , 2011, Annual review of entomology.

[59]  Owen L. Petchey,et al.  Interaction strengths in food webs: issues and opportunities , 2004 .

[60]  T. Knight THE EFFECTS OF HERBIVORY AND POLLEN LIMITATION ON A DECLINING POPULATION OF TRILLIUM GRANDIFLORUM , 2004 .

[61]  J. Addicott Stability properties of 2-species models of mutualism: Simulation studies , 1981, Oecologia.

[62]  M. Emmerson,et al.  Predator–prey body size, interaction strength and the stability of a real food web , 2004 .

[63]  M. Gilpin,et al.  Perturbation Experiments in Community Ecology: Theory and Practice , 1984 .

[64]  Guy Woodward,et al.  Body size in ecological networks. , 2005, Trends in ecology & evolution.

[65]  Mark Novak,et al.  Estimating nonlinear interaction strengths: an observation-based method for species-rich food webs. , 2008, Ecology.

[66]  P. Abrams,et al.  On classifying interactions between populations , 1987, Oecologia.

[67]  M. Pettersson,et al.  Pollination by a guild of fluctuating moth populations : option for unspecialization in Silene vulgaris , 1991 .

[68]  Richard Levins,et al.  Life expectancy change in perturbed communities: derivation and qualitative analysis. , 2005, Mathematical biosciences.

[69]  J. Timothy Wootton,et al.  THEORETICAL CONCEPTS AND EMPIRICAL APPROACHES TO MEASURING INTERACTION STRENGTH , 1998 .

[70]  Rampal S Etienne,et al.  Phenology drives mutualistic network structure and diversity. , 2012, Ecology letters.

[71]  Breno M. Freitas,et al.  Wild Pollinators Enhance Fruit Set of Crops Regardless of Honey Bee Abundance , 2013, Science.

[72]  Donald L DeAngelis,et al.  A consumer-resource approach to the density-dependent population dynamics of mutualism. , 2010, Ecology.

[73]  H. Sahli,et al.  Characterizing ecological generalization in plant-pollination systems , 2006, Oecologia.

[74]  Tamar Frankel [The theory and the practice...]. , 2001, Tijdschrift voor diergeneeskunde.

[75]  W. Morris,et al.  Benefit and cost curves for typical pollination mutualisms. , 2010, Ecology.

[76]  Rodrigo Ramos-Jiliberto,et al.  Topological plasticity increases robustness of mutualistic networks. , 2012, The Journal of animal ecology.

[77]  T. Okuyama,et al.  Network structural properties mediate the stability of mutualistic communities. , 2008, Ecology letters.

[78]  T. Knight,et al.  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 , 2010, Plant Ecology.

[79]  R. May,et al.  Stability and Complexity in Model Ecosystems , 1976, IEEE Transactions on Systems, Man, and Cybernetics.

[80]  J. Bronstein Our Current Understanding of Mutualism , 1994, The Quarterly Review of Biology.

[81]  P. Jordano,et al.  Seed dispersal effectiveness revisited: a conceptual review. , 2010, The New phytologist.

[82]  P. Jordano,et al.  SEED DISPERSER EFFECTIVENESS: THE QUANTITY COMPONENT AND PATTERNS OF SEED RAIN FOR PRUNUS MAHALEB , 2000 .

[83]  R. Briers,et al.  Ecology: From Individuals to Ecosystems , 2006 .

[84]  Jane Memmott,et al.  The impact of an alien plant on a native plant-pollinator network: an experimental approach. , 2007, Ecology letters.

[85]  C. Horvitz,et al.  Variation Among Floral Visitors in Pollination Ability: A Precondition for Mutualism Specialization , 1984, Science.

[86]  P. Yodzis,et al.  Body Size and Consumer-Resource Dynamics , 1992, The American Naturalist.

[87]  A. Hastings,et al.  Weak trophic interactions and the balance of nature , 1998, Nature.

[88]  Jeffrey M Dambacher,et al.  UNDERSTANDING AND PREDICTING EFFECTS OF MODIFIED INTERACTIONS THROUGH A QUALITATIVE ANALYSIS OF COMMUNITY STRUCTURE , 2007, The Quarterly Review of Biology.

[89]  R. Paine,et al.  Food-web analysis through field measurement of per capita interaction strength , 1992, Nature.

[90]  Carlos J. Melián,et al.  The nested assembly of plant–animal mutualistic networks , 2003, Proceedings of the National Academy of Sciences of the United States of America.