How to be a specialist? Quantifying specialisation in pollination networks

The analysis of ecological networks has gained a very prominent foothold in ecology over the last years. While many publications try to elucidate patterns about the networks, others are primarily concerned with the role of specific species in the network. The core challenge here is to tell specialists from generalists. While field data and observations can be used to directly assess specialisation levels, the indirect way through networks is burdened with problems. Here, I review eight measures to quantify specialisation in pollination networks (degree, node specialisation, betweenness, closeness, strength, pollination support, Shannon’s H and discrimination d’), the first four being based on binary, the others on weighted network data. All data and R-code are available as supplement and can be applied beyond pollination networks. The indices convey different concepts of specialisation and hence quantify different aspects. Still, there is some redundancy, with node specialisation and closeness quantifying the same properties, as do degree, betweenness and Shannon’s H. Using artificial and real network data, I illustrate the interpretation of the different indices and the importance of using a null model to correct for expectations given the different observed frequencies of interactions. For a well-described network the distributions of specialisation values do not differ from null model expectations for most indices. Finally, I investigate the effect of cattle grazing on the specialisation of an important pollinator in eight replicated pollination networks as an illustration of how to employ the specialisation indices, null models and permutation-based statistics in the analysis of specialisation in pollination networks.

[1]  J. Harper Population Biology of Plants , 1979 .

[2]  T. Ashman,et al.  A quantitative synthesis of pollen supplementation experiments highlights the contribution of resource reallocation to estimates of pollen limitation. , 2006, American journal of botany.

[3]  Martin G. Everett,et al.  A Graph-theoretic perspective on centrality , 2006, Soc. Networks.

[4]  A. Klein,et al.  Caveats to quantifying ecosystem services: fruit abortion blurs benefits from crop pollination. , 2007, Ecological applications : a publication of the Ecological Society of America.

[5]  Carsten F. Dormann,et al.  Introducing the bipartite Package: Analysing Ecological Networks , 2008 .

[6]  S. Schittenhelm,et al.  Efficiency of various insects in germplasm regeneration of carrot, onion and turnip rape accessions , 1997 .

[7]  János Podani,et al.  RANDOMIZATION OF PRESENCE–ABSENCE MATRICES: COMMENTS AND NEW ALGORITHMS , 2004 .

[8]  A. Timmermann,et al.  Pollination networks and functional specialization: a test using Lesser Antillean plant–hummingbird assemblages , 2008 .

[9]  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.

[10]  Juan M Morales,et al.  Invasive Mutualists Erode Native Pollination Webs , 2008, PLoS biology.

[11]  R. Alarcón Congruence between visitation and pollen‐transport networks in a California plant–pollinator community , 2010 .

[12]  Louis-Félix Bersier,et al.  QUANTITATIVE DESCRIPTORS OF FOOD-WEB MATRICES , 2002 .

[13]  J. Ollerton,et al.  Multiple meanings and modes: on the many ways to be a generalist flower , 2007 .

[14]  W. Patefield,et al.  An Efficient Method of Generating Random R × C Tables with Given Row and Column Totals , 1981 .

[15]  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.

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

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

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

[19]  N. Waser Flower Constancy: Definition, Cause, and Measurement , 1986, The American Naturalist.

[20]  M. Aizen,et al.  Plant reproductive susceptibility to habitat fragmentation: review and synthesis through a meta-analysis. , 2006, Ecology letters.

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

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

[23]  R. Reynolds,et al.  Nectar reward and advertisement in hummingbird-pollinated Silene virginica (Caryophyllaceae). , 2006, American journal of botany.

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

[25]  Michele R. Dudash,et al.  Pollination Syndromes and Floral Specialization , 2004 .

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

[27]  W. Kunin Sex and the single mustard : population density and pollinator behavior effects on seed-set , 1993 .

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

[29]  K. Lunau Adaptive radiation and coevolution — pollination biology case studies , 2004 .

[30]  L. Freeman Centrality in social networks conceptual clarification , 1978 .

[31]  M. C. Tellería,et al.  Bombus species and their associated flora in Argentina , 2001 .

[32]  Michele R. Dudash,et al.  Pollen Limitation of Plant Reproduction: Pattern and Process , 2005 .

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

[34]  N. Blüthgen,et al.  Pollinator diversity and specialization in relation to flower diversity , 2010 .

[35]  L. Jost Entropy and diversity , 2006 .

[36]  J. Willis,et al.  Is floral diversification associated with pollinator divergence? Flower shape, flower colour and pollinator preference in Chilean Mimulus. , 2008, Annals of botany.

[37]  Neal M. Williams,et al.  Crop pollination from native bees at risk from agricultural intensification , 2002, Proceedings of the National Academy of Sciences of the United States of America.

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

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

[40]  Jaboury Ghazoul,et al.  Buzziness as usual? Questioning the global pollination crisis. , 2005, Trends in ecology & evolution.

[41]  Carsten F. Dormann,et al.  Indices, Graphs and Null Models: Analyzing Bipartite Ecological Networks , 2009 .

[42]  S. Hurlbert The Measurement of Niche Overlap and Some Relatives , 1978 .

[43]  Diego P. Vázquez,et al.  Changes in interaction biodiversity induced by an introduced ungulate , 2003 .

[44]  R. Fisher,et al.  The Relation Between the Number of Species and the Number of Individuals in a Random Sample of an Animal Population , 1943 .

[45]  P. Kron,et al.  Self-compatibility, autonomous self-pollination, and insect-mediated pollination in the clonal species Iris versicolor , 1993 .

[46]  H. Shaffer,et al.  Annual review of ecology, evolution, and systematics , 2003 .

[47]  Nico Blüthgen,et al.  Why network analysis is often disconnected from community ecology: A critique and an ecologist's guide , 2010 .

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

[49]  Jens M. Olesen,et al.  Centrality measures and the importance of generalist species in pollination networks , 2010 .

[50]  K. Burns Network properties of an epiphyte metacommunity , 2007 .