Uniting pattern and process in plant-animal mutualistic networks: a review.

BACKGROUND Ecologists and evolutionary biologists are becoming increasingly interested in networks as a framework to study plant-animal mutualisms within their ecological context. Although such focus on networks has brought about important insights into the structure of these interactions, relatively little is still known about the mechanisms behind these patterns. SCOPE The aim in this paper is to offer an overview of the mechanisms influencing the structure of plant-animal mutualistic networks. A brief summary is presented of the salient network patterns, the potential mechanisms are discussed and the studies that have evaluated them are reviewed. This review shows that researchers of plant-animal mutualisms have made substantial progress in the understanding of the processes behind the patterns observed in mutualistic networks. At the same time, we are still far from a thorough, integrative mechanistic understanding. We close with specific suggestions for directions of future research, which include developing methods to evaluate the relative importance of mechanisms influencing network patterns and focusing research efforts on selected representative study systems throughout the world.

[1]  H. Pulliam On the relationship between niche and distribution , 2000 .

[2]  Albert,et al.  Emergence of scaling in random networks , 1999, Science.

[3]  Jordi Bascompte,et al.  Plant-Animal Mutualistic Networks: The Architecture of Biodiversity , 2007 .

[4]  Paulo S. Oliveira,et al.  The ecology and evolution of ant-plant interactions , 2007 .

[5]  Luis Santamaría,et al.  Linkage Rules for Plant–Pollinator Networks: Trait Complementarity or Exploitation Barriers? , 2007, PLoS biology.

[6]  Owen L. Petchey,et al.  Foraging biology predicts food web complexity , 2006, Proceedings of the National Academy of Sciences.

[7]  Jordi Bascompte,et al.  The ecological consequences of complex topology and nested structure in pollination webs. , 2006 .

[8]  J. Thompson,et al.  The Coevolutionary Process , 1994 .

[9]  Jordi Bascompte,et al.  A neutral‐niche theory of nestedness in mutualistic networks , 2008 .

[10]  D. Vázquez,et al.  The effect of space in plant–animal mutualistic networks: insights from a simulation study , 2008 .

[11]  D. Simberloff,et al.  Ecological Specialization and Susceptibility to Disturbance: Conjectures and Refutations , 2002, The American Naturalist.

[12]  Jeff Ollerton,et al.  The pollination ecology of an assemblage of grassland asclepiads in South Africa. , 2003, Annals of botany.

[13]  Paulo R. Guimarães,et al.  Interaction Intimacy Affects Structure and Coevolutionary Dynamics in Mutualistic Networks , 2007, Current Biology.

[14]  J. Thompson The Geographic Mosaic of Coevolution , 2005 .

[15]  Paulo R Guimarães,et al.  Asymmetries in specialization in ant–plant mutualistic networks , 2006, Proceedings of the Royal Society B: Biological Sciences.

[16]  J. Bascompte,et al.  Ecological networks : beyond food webs Ecological networks – beyond food webs , 2008 .

[17]  C. Fontaine,et al.  Generalist foraging of pollinators: diet expansion at high density , 2008 .

[18]  Jordi Bascompte,et al.  The smallest of all worlds: pollination networks. , 2006, Journal of theoretical biology.

[19]  R. Solé,et al.  Topological properties of food webs: from real data to community assembly models Oikos 102 , 2003 .

[20]  Diego P. Vázquez,et al.  ASYMMETRIC SPECIALIZATION: A PERVASIVE FEATURE OF PLANT-POLLINATOR INTERACTIONS , 2004 .

[21]  P. Klinkhamer,et al.  Asymmetric specialization and extinction risk in plant–flower visitor webs: a matter of morphology or abundance? , 2007, Oecologia.

[22]  Joseph Tzanopoulos,et al.  Long-term observation of a pollination network: fluctuation in species and interactions, relative invariance of network structure and implications for estimates of specialization. , 2008, Ecology letters.

[23]  Owen L Petchey,et al.  Size, foraging, and food web structure , 2008, Proceedings of the National Academy of Sciences.

[24]  Jordi Bascompte,et al.  Build-up mechanisms determining the topology of mutualistic networks. , 2007, Journal of theoretical biology.

[25]  Theodora Petanidou,et al.  MEASURING BEE DIVERSITY IN DIFFERENT EUROPEAN HABITATS AND BIOGEOGRAPHICAL REGIONS , 2008 .

[26]  Jordi Bascompte,et al.  Non-random coextinctions in phylogenetically structured mutualistic networks , 2007, Nature.

[27]  Pedro Jordano,et al.  GEOGRAPHIC PATTERNS IN PLANT–POLLINATOR MUTUALISTIC NETWORKS , 2002 .

[28]  J. Lawton,et al.  Insects on Plants , 1984 .

[29]  Rebecca E. Irwin,et al.  Ecological and Evolutionary Consequences of Multispecies Plant-Animal Interactions , 2004 .

[30]  J. Bronstein,et al.  The evolution of plant-insect mutualisms. , 2006, The New phytologist.

[31]  Carsten F. Dormann,et al.  Ecological networks - foodwebs and beyond , 2009 .

[32]  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.

[33]  P. Klinkhamer,et al.  Size constraints and flower abundance determine the number of interactions in a plant /flower visitor web , 2006 .

[34]  N. Bartoloni,et al.  A year‐long plant‐pollinator network , 2006 .

[35]  C. Combes,et al.  Parasitism: The Ecology and Evolution of Intimate Interactions , 2001 .

[36]  D. Schemske,et al.  Geographic patterns in plant-pollinator mutualistic networks: Comment , 2004 .

[37]  M. Devoto,et al.  Patterns of interaction between plants and pollinators along an environmental gradient , 2005 .

[38]  Lynn V. Dicks,et al.  Compartmentalization in plant–insect flower visitor webs , 2002 .

[39]  J. Bascompte,et al.  Invariant properties in coevolutionary networks of plant-animal interactions , 2002 .

[40]  M. Aizen,et al.  Chapter 9 Community-Wide Patterns of Specialization in Plant – Pollinator Interactions Revealed by Null Models , 2004 .

[41]  J. Ollerton,et al.  Pollination niche overlap between a parasitic plant and its host , 2007, Oecologia.

[42]  J Memmott,et al.  The structure of a plant-pollinator food web. , 1999, Ecology letters.

[43]  J. Bascompte,et al.  Effects of phenotypic complementarity and phylogeny on the nested structure of mutualistic networks , 2007 .

[44]  Neal M. Williams,et al.  Species abundance and asymmetric interaction strength in ecological networks , 2007 .

[45]  J. Bascompte,et al.  The modularity of pollination networks , 2007, Proceedings of the National Academy of Sciences.

[46]  Jochen Fründ,et al.  What do interaction network metrics tell us about specialization and biological traits? , 2008, Ecology.

[47]  N. Blüthgen,et al.  Ant-hemipteran trophobioses in a Bornean rainforest – diversity, specificity and monopolisation , 2006, Insectes Sociaux.

[48]  Jordi Bascompte,et al.  Random initial condition in small Barabasi-Albert networks and deviations from the scale-free behavior. , 2005, Physical review. E, Statistical, nonlinear, and soft matter physics.

[49]  Dawn M. Kaufman,et al.  LATITUDINAL GRADIENTS OF BIODIVERSITY:Pattern,Process,Scale,and Synthesis , 2003 .

[50]  A. Ives,et al.  Phylogenetic Analysis of Trophic Associations , 2006, The American Naturalist.

[51]  Jeff Ollerton,et al.  Year‐to‐year variation in the topology of a plant–pollinator interaction network , 2008 .

[52]  Graham Bell,et al.  The Distribution of Abundance in Neutral Communities , 2000, The American Naturalist.

[53]  A. J. Moore,et al.  Selection, Inheritance, and the Evolution of Parent‐Offspring Interactions , 2004, The American Naturalist.

[54]  Jonathan M. Chase,et al.  Ecological Niches: Linking Classical and Contemporary Approaches , 2003 .

[55]  Stefano Allesina,et al.  A General Model for Food Web Structure , 2008, Science.

[56]  K. Burns A simple null model predicts fruit‐frugivore interactions in a temperate rainforest , 2006 .

[57]  D. Snow,et al.  Feeding niches of hummingbirds in a Trinidad valley , 1972 .

[58]  S. Hubbell,et al.  The unified neutral theory of biodiversity and biogeography at age ten. , 2011, Trends in ecology & evolution.

[59]  Jane Memmott,et al.  Tolerance of pollination networks to species extinctions , 2004, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[60]  É. Thébault,et al.  Does asymmetric specialization differ between mutualistic and trophic networks , 2008 .

[61]  N. Blüthgen,et al.  Measuring specialization in species interaction networks , 2006, BMC Ecology.

[62]  C. Herrera Plant-vertebrate seed dispersal systems in the Mediterranean : ecological, evolutionary, and historical determinants , 1995 .

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

[64]  Diego P. Vázquez,et al.  Degree distribution in plant–animal mutualistic networks: forbidden links or random interactions? , 2005 .

[65]  C. Herrera,et al.  Historical Effects and Sorting Processes as Explanations for Contemporary Ecological Patterns: Character Syndromes in Mediterranean Woody Plants , 1992, The American Naturalist.

[66]  R. Poulin Evolutionary Ecology of Parasites , 1997 .

[67]  N. Waser,et al.  Size-specific interaction patterns and size matching in a plant-pollinator interaction web. , 2009, Annals of botany.

[68]  Lars Chittka,et al.  Generalization in Pollination Systems, and Why it Matters , 1996 .

[69]  Neo D. Martinez,et al.  Food-web structure and network theory: The role of connectance and size , 2002, Proceedings of the National Academy of Sciences of the United States of America.

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

[71]  Pedro Jordano,et al.  Patterns of Mutualistic Interactions in Pollination and Seed Dispersal: Connectance, Dependence Asymmetries, and Coevolution , 1987, The American Naturalist.

[72]  D. Vázquez,et al.  The Latitudinal Gradient in Niche Breadth: Concepts and Evidence , 2004, The American Naturalist.

[73]  Nils Blüthgen,et al.  Specialization, Constraints, and Conflicting Interests in Mutualistic Networks , 2007, Current Biology.

[74]  C. Pélabon Plant–Pollinator Interactions: From Specialization to Generalization, Nickolas M. Waser, Jeff Ollerton (Eds.). University of Chicago Press, Chicago (2006), Pp. 445. Price $45.00 , 2006 .

[75]  C. Herrera,et al.  Plant generalization on pollinators: species property or local phenomenon? , 2005, American journal of botany.

[76]  C. Fonseca,et al.  Asymmetries, compartments and null interactions in an Amazonian ant-plant community , 1996 .

[77]  Jens M. Olesen,et al.  Structure of a plant–flower‐visitor network in the high‐altitude sub‐alpine desert of Tenerife, Canary Islands , 2003 .

[78]  R. Ricklefs,et al.  Community Diversity: Relative Roles of Local and Regional Processes , 1987, Science.

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

[80]  Jeff Ollerton,et al.  Plant-pollinator interactions: from specialization to generalization. , 2005 .

[81]  Diego P. Vázquez,et al.  NULL MODEL ANALYSES OF SPECIALIZATION IN PLANT–POLLINATOR INTERACTIONS , 2003 .

[82]  Jeff Ollerton,et al.  Latitudinal trends in plant‐pollinator interactions: are tropical plants more specialised? , 2002 .

[83]  J. Bascompte,et al.  Structure in plant–animal interaction assemblages , 2006 .

[84]  S. Chamberlain,et al.  Body size predicts degree in ant–plant mutualistic networks , 2009 .

[85]  Jordi Bascompte,et al.  Ecological networks, nestedness and sampling effort , 2007 .

[86]  Paulo R. Guimarães,et al.  On nestedness analyses: rethinking matrix temperature and anti‐nestedness , 2007 .

[87]  G. Bell Neutral macroecology. , 2001, Science.

[88]  Luciano Cagnolo,et al.  Evaluating multiple determinants of the structure of plant-animal mutualistic networks. , 2009, Ecology.

[89]  Jordi Bascompte,et al.  Temporal dynamics in a pollination network. , 2008, Ecology.

[90]  Horacio Ceva,et al.  Analysis and assembling of network structure in mutualistic systems. , 2007, Journal of theoretical biology.