Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Pollinator interaction flexibility across scales affects patch colonization and occupancy

Nature Ecology & Evolution volume 5, pages 787–793 (2021)Cite this article

Subjects

Abstract

Global change alters ecological communities and may disrupt ecological interactions and the provision of ecosystem functions. As ecological communities respond to global change, species may either go locally extinct or form novel interactions. To date, few studies have assessed how flexible species are in their interaction patterns, mainly due to the scarcity of data spanning long time series. Using a ten-year species-level dataset on the assembly of mutualistic networks from the Central Valley in California, we test whether interaction flexibility affects pollinators’ colonization and persistence and their resulting habitat occupancy in a highly modified landscape. We propose three metrics of interaction flexibility associated with different scales of organization within ecological communities and explore which species’ traits affect them. Our results provide empirical evidence linking species’ ability to colonize habitat patches across a landscape to the role they play in networks. Phenological breadth and body size had contrasting effects on interaction flexibility. We demonstrate the relationship between mutualistic networks and species’ ability to colonize and persist in the landscape, suggesting interaction flexibility as a potential mechanism for communities to maintain ecosystem function despite changes in community composition.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Diagram representing the different scales for which we calculated interaction flexibility.
Fig. 2: Partner, role and structural flexibility for the 31 species seen more than three times at a site included in the analyses.
Fig. 3: The effect of partner variability, role variability and structural variability on persistence (solid line), colonization (dashed line) and proportion of occupied patches (dotted line) across the landscape.

Similar content being viewed by others

Data availability

Data describing plant–pollinator interactions as well as data generated in this study are available in Github (https://github.com/Magaiarsa/intFlex) and Zenodo (https://zenodo.org/record/4485996#.YE9dzGRKhhF).

Code availability

Code is deposited in Github (https://github.com/Magaiarsa/intFlex) and Zenodo (https://zenodo.org/record/4485996#.YE9dzGRKhhF).

References

  1. Kaiser-Bunbury, C. N. et al. Ecosystem restoration strengthens pollination network resilience and function. Nature 542, 223–227 (2017).

    Article  CAS  PubMed  Google Scholar 

  2. Newbold, T. et al. Global effects of land use on local terrestrial biodiversity. Nature 520, 45–50 (2015).

    Article  CAS  PubMed  Google Scholar 

  3. Memmott, J., Waser, N. M. & Price, M. V. Tolerance of pollination networks to species extinctions. Proc. R. Soc. B 271, 2605–2611 (2004).

    Article  PubMed  Google Scholar 

  4. Kaiser-Bunbury, C. N., Muff, S., Memmott, J., Müller, C. B. & Caflisch, A. The robustness of pollination networks to the loss of species and interactions: a quantitative approach incorporating pollinator behaviour. Ecol. Lett. 13, 442–452 (2010).

    Article  PubMed  Google Scholar 

  5. Ponisio, L. C., Gaiarsa, M. P. & Kremen, C. Opportunistic attachment assembles plant–pollinator networks. Ecol. Lett. 20, 1261–1272 (2017).

    Article  PubMed  Google Scholar 

  6. Spiesman, B. J. & Gratton, C. Flexible foraging shapes the topology of plant–pollinator interaction networks. Ecology 97, 1431–1441 (2016).

    Article  PubMed  Google Scholar 

  7. CaraDonna, P. J. et al. Interaction rewiring and the rapid turnover of plant–pollinator networks. Ecol. Lett. 20, 385–394 (2017).

  8. Tylianakis, J. M., Martínez-García, L. B., Richardson, S. J., Peltzer, D. A. & Dickie, I. A. Symmetric assembly and disassembly processes in an ecological network. Ecol. Lett. 21, 896–904 (2018).

    Article  PubMed  Google Scholar 

  9. Yeakel, J. D. et al. Collapse of an ecological network in Ancient Egypt. Proc. Natl Acad. Sci. USA 111, 14472–14477 (2014).

    Article  CAS  PubMed  Google Scholar 

  10. Burkle, L. A. & Alarcón, R. The future of plant–pollinator diversity: understanding interaction networks across time, space, and global change. Am. J. Bot. 98, 528–538 (2011).

    Article  PubMed  Google Scholar 

  11. Cardinale, B. J. et al. Biodiversity loss and its impact on humanity. Nature 486, 59–67 (2012).

    Article  CAS  PubMed  Google Scholar 

  12. Tylianakis, J. M. & Morris, R. J. Ecological networks across environmental gradients. Annu. Rev. Ecol. Syst. 48, 24–48 (2017).

  13. Bascompte, J. & Jordano, P. Mutualistic Networks (Princeton Univ. Press, 2013).

  14. MacLeod, M., Genung, M. A., Ascher, J. S. & Winfree, R. Measuring partner choice in plant–pollinator networks: using null models to separate rewiring and fidelity from chance. Ecology 97, 2925–2931 (2016).

    Article  PubMed  Google Scholar 

  15. Fortuna, M. A., Nagavci, A., Barbour, M. A. & Bascompte, J. Partner fidelity and asymmetric specialization in ecological networks. Am. Nat. 196, 382–389 (2020).

  16. Bascompte, J. & Stouffer, D. B. The assembly and disassembly of ecological networks. Philos. Trans. R. Soc. B 364, 1781 (2009).

    Article  Google Scholar 

  17. Cirtwill, A. R., Roslin, T., Rasmussen, C., Olesen, J. M. & Stouffer, D. B. Between-year changes in community composition shape species’ roles in an Arctic plant–pollinator network. Oikos 127, 1163–1176 (2018).

  18. Mora, B. B., Shin, E., CaraDonna, P. J. & Stouffer, D. B. Untangling the seasonal dynamics of plant–pollinator communities. Nat. Commun. 11, 4086 (2020).

  19. Saavedra, S., Stouffer, D. B., Uzzi, B. & Bascompte, J. Strong contributors to network persistence are the most vulnerable to extinction. Nature 478, 233–235 (2011).

    Article  CAS  PubMed  Google Scholar 

  20. Sebastián-González, E. Drivers of species role in avian seed-dispersal mutualistic networks. J. Anim. Ecol. 86, 878–887 (2017).

    Article  PubMed  Google Scholar 

  21. Oliver, T. H. et al. Biodiversity and resilience of ecosystem functions. Trends Ecol. Evol. 30, 673–684 (2015).

    Article  PubMed  Google Scholar 

  22. CaraDonna, P. J. et al. Seeing through the static: the temporal dimension of plant–animal mutualistic interactions. Ecol. Lett. 24, 149–161 (2020).

  23. Vázquez, D. P., Chacoff, N. P. & Cagnolo, L. Evaluating multiple determinants of the structure of plant–animal mutualistic networks. Ecology 90, 2039–2046 (2009).

    Article  PubMed  Google Scholar 

  24. Vázquez, D. P., Blüthgen, N., Cagnolo, L. & Chacoff, N. P. Uniting pattern and process in plant–animal mutualistic networks: a review. Ann. Bot. 103, 1445–1457 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  25. Olesen, J. M., Bascompte, J., Dupont, Y. & Jordano, P. The modularity of pollination networks. Proc. Natl Acad. Sci. USA 104, 19891–19896 (2007).

    Article  CAS  PubMed  Google Scholar 

  26. Brosi, B. J. & Briggs, H. M. Single pollinator species losses reduce floral fidelity and plant reproductive function. Proc. Natl Acad. Sci. USA 110, 13044–13048 (2013).

    Article  CAS  PubMed  Google Scholar 

  27. Valdovinos, F. S. et al. Niche partitioning due to adaptive foraging reverses effects of nestedness and connectance on pollination network stability. Ecol. Lett. 19, 1277–1286 (2016).

    Article  PubMed  Google Scholar 

  28. Rafferty, N. E., CaraDonna, P. J. & Bronstein, J. L. Phenological shifts and the fate of mutualisms. Oikos 124, 14–21 (2015).

    Article  PubMed  Google Scholar 

  29. Winfree, R., Williams, N. M., Dushoff, J. & Kremen, C. Species abundance, not diet breadth, drives the persistence of the most linked pollinators as plant–pollinator networks disassemble. Am. Nat. 183, 600–611 (2014).

    Article  PubMed  Google Scholar 

  30. Benjamin, F. E., Reilly, J. R. & Winfree, R. Pollinator body size mediates the scale at which land use drives crop pollination services. J. Appl. Ecol. 51, 440–449 (2014).

    Article  Google Scholar 

  31. Grab, H. et al. Habitat enhancements rescue bee body size from the negative effects of landscape simplification. J. Appl. Ecol. 56, 2144–2154 (2019).

    Article  Google Scholar 

  32. Fontaine, C., Collin, C. L. & Dajoz, I. Generalist foraging of pollinators: diet expansion at high density. J. Ecol. 96, 1002–1010 (2008).

    Article  Google Scholar 

  33. Stouffer, D. B., Sales-Pardo, M., Sirer, M. I. & Bascompte, J. Evolutionary conservation of species’ roles in food webs. Science 335, 1489–1492 (2012).

    Article  CAS  PubMed  Google Scholar 

  34. Simmons, B. I. et al. Motifs in bipartite ecological networks: uncovering indirect interactions. Oikos 128, 154–170 (2019).

    Article  Google Scholar 

  35. Ponisio, L. C. Pyrodiversity promotes interaction complementarity and population resistance. Ecol. Evol. 10, 4431–4447 (2020).

    Article  PubMed  PubMed Central  Google Scholar 

  36. Grab, H., Blitzer, E. J., Danforth, B., Loeb, G. & Poveda, K. Temporally dependent pollinator competition and facilitation with mass flowering crops affects yield in co-blooming crops. Sci. Rep. 7, 45296 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. MacArthur, R. H. & Pianka, E. R. On optimal use of a patchy environment. Am. Nat. 100, 603–609 (1966).

    Article  Google Scholar 

  38. Mitchell, W. A. An optimal control theory of diet selection: the effects of resource depletion and exploitative competition. Oikos 58, 16–24 (1990).

  39. Robinson, B. W. & Wilson, D. S. Optimal foraging, specialization, and a solution to Liem’s paradox. Am. Nat. 151, 223–235 (1998).

    Article  CAS  PubMed  Google Scholar 

  40. Valdovinos, F. S., Moisset de Espanés, P., Flores, J. D. & Ramos-Jiliberto, R. Adaptive foraging allows the maintenance of biodiversity of pollination networks. Oikos 122, 907–917 (2013).

    Article  Google Scholar 

  41. Ponisio, L. C. et al. A network perspective for community assembly. Front. Ecol. Environ. 7, 103 (2019).

    Article  Google Scholar 

  42. Benadi, G. & Gegear, R. J. Adaptive foraging of pollinators can promote pollination of a rare plant species. Am. Nat. 192, E81–E92 (2018).

    Article  PubMed  Google Scholar 

  43. Vaudo, A. D., Patch, H. M., Mortensen, D. A., Tooker, J. F. & Grozinger, C. M. Macronutrient ratios in pollen shape bumble bee (Bombus impatiens) foraging strategies and floral preferences. Proc. Natl Acad. Sci. USA 113, E4035–E4042 (2016).

    Article  CAS  PubMed  Google Scholar 

  44. Poisot, T., Stouffer, D. B. & Gravel, D. Beyond species: why ecological interaction networks vary through space and time. Oikos 124, 243–251 (2015).

    Article  Google Scholar 

  45. Fort, H., Vázquez, D. P. & Lan, B. L. Abundance and generalisation in mutualistic networks: solving the chicken-and-egg dilemma. Ecol. Lett. 19, 4–11 (2016).

    Article  PubMed  Google Scholar 

  46. Bascompte, J., Jordano, P., Melián, C. J. & Olesen, J. M. The nested assembly of plant–animal mutualistic networks. Proc. Natl Acad. Sci. USA 100, 9383–9387 (2003).

    Article  CAS  PubMed  Google Scholar 

  47. Lever, J. J., van Nes, E. H., Scheffer, M. & Bascompte, J. The sudden collapse of pollinator communities. Ecol. Lett. 17, 350–359 (2014).

    Article  PubMed  Google Scholar 

  48. Bascompte, J. & Ferrera, A. in Theoretical Ecology: Concepts and Applications (eds McCann, A. S. & Gellner, G.) 93–115 (Oxford Univ. Press, 2020).

  49. Allesina, S. & Tang, S. Stability criteria for complex ecosystems. Nature 483, 205–208 (2012).

    Article  CAS  PubMed  Google Scholar 

  50. Suweis, S., Simini, F., Banavar, J. R. & Maritan, A. Emergence of structural and dynamical properties of ecological mutualistic networks. Nature 500, 449–452 (2013).

    Article  CAS  PubMed  Google Scholar 

  51. Naeem, S. & Li, S. Biodiversity enhances ecosystem reliability. Nature 390, 507–509 (1997).

    Article  CAS  Google Scholar 

  52. Winfree, R. et al. Species turnover promotes the importance of bee diversity for crop pollination at regional scales. Science 359, 791–793 (2018).

    Article  CAS  PubMed  Google Scholar 

  53. Kremen, C. & M’Gonigle, L. K. Small-scale restoration in intensive agricultural landscapes supports more specialized and less mobile pollinator species. J. Appl. Ecol. 52, 602–610 (2015).

    Article  Google Scholar 

  54. Kremen, C., Williams, N. & Thorp, R. Crop pollination from native bees at risk from agricultural intensification. Proc. Natl Acad. Sci. USA 99, 16812–16816 (2002).

  55. Morandin, L., Long, R. & Kremen, C. Pest control and pollination cost–benefit analysis of hedgerow restoration in a simplified agricultural landscape. J. Econ. Entomol. 109, 1020–1027 (2016).

    Article  CAS  PubMed  Google Scholar 

  56. Brittain, C., Williams, N., Kremen, C. & Klein, A. Synergistic effects of non-Apis bees and honey bees for pollination services. Proc. R. Soc. B 280, 1471–2954 (2013).

    Article  Google Scholar 

  57. Chao, A., Chazdon, R. L., Colwell, R. K. & Shen, T.-J. A new statistical approach for assessing similarity of species composition with incidence and abundance data. Ecol. Lett. 8, 148–159 (2005).

    Article  Google Scholar 

  58. Oksanen, J. et al. vegan: Community Ecology Package (2019); https://CRAN.R-project.org/package=vegan

  59. Anderson, M. J. et al. Navigating the multiple meanings of β diversity: a roadmap for the practicing ecologist. Ecol. Lett. 14, 19–28 (2011).

    Article  PubMed  Google Scholar 

  60. Anderson, M. J., Ellingsen, K. E. & McArdle, B. H. Multivariate dispersion as a measure of beta diversity. Ecol. Lett. 9, 683–693 (2006).

    Article  PubMed  Google Scholar 

  61. Mora, B. B., Cirtwill, A. R. & Stouffer, D. B. pymfinder: a tool for the motif analysis of binary and quantitative complex networks (2018); https://doi.org/10.1101/364703

  62. Simmons, B. I. et al. bmotif: a package for motif analyses of bipartite networks. Methods Ecol. Evol. 10, 695–701 (2019).

    Article  Google Scholar 

  63. Anderson, M. J. A new method for non-parametric multivariate analysis of variance. Austral Ecol. 26, 32–46 (2001).

    Google Scholar 

  64. Baker, N. J., Kaartinen, R., Roslin, T. & Stouffer, D. B. Species’ roles in food webs show fidelity across a highly variable oak forest. Ecography 38, 130–139 (2015).

    Article  Google Scholar 

  65. Bastolla, U. et al. The architecture of mutualistic networks minimizes competition and increases biodiversity. Nature 458, 1018–1020 (2009).

    Article  CAS  PubMed  Google Scholar 

  66. Dormann, C., Gruber, B. & Fründ, J. Introducing the bipartite package: analysing ecological networks. R News 8, 8 (2008).

    Google Scholar 

  67. Dorazio, R. M., Kery, M., Royle, J. A. & Plattner, M. Models for inference in dynamic metacommunity systems. Ecology 91, 2466–2475 (2010).

    Article  PubMed  Google Scholar 

  68. Ponisio, L. C., de Valpine, P., M’Gonigle, L. K. & Kremen, C. Proximity of restored hedgerows interacts with local floral diversity and species’ traits to shape long-term pollinator metacommunity dynamics. Ecol. Lett. 22, 1048–1060 (2019).

    Article  PubMed  Google Scholar 

  69. Royle, J. A. & Kéry, M. A Bayesian state–space formulation of dynamic occupancy models. Ecology 88, 1813–1823 (2007).

    Article  PubMed  Google Scholar 

  70. Ponisio, L. C., de Valpine, P., Michaud, N. & Turek, D. One size does not fit all: customizing MCMC methods for hierarchical models using NIMBLE. Ecol. Evol. 10, 2385–2416 (2020).

    Article  PubMed  PubMed Central  Google Scholar 

  71. de Valpine, P. et al. Programming with models: writing statistical algorithms for general model structures with NIMBLE. J. Comput. Graph. Stat. 26, 403–413 (2017).

    Article  Google Scholar 

  72. Shipley, B. Cause and Correlation in Biology: A User’s Guide to Path Analysis, Structural Equations and Causal Inference (Cambridge Univ. Press, 2004).

  73. Kremen, C., M’Gonigle, L. K. & Ponisio, L. C. Pollinator community assembly tracks changes in floral resources as restored hedgerows mature in agricultural landscapes. Front. Ecol. Evol. 6, 170 (2018).

    Article  Google Scholar 

  74. Ponisio, L. C., M’gonigle, L. K. & Kremen, C. On-farm habitat restoration counters biotic homogenization in intensively managed agriculture. Glob. Change Biol. 22, 704–715 (2016).

    Article  Google Scholar 

  75. Lefcheck, J. S. PiecewiseSEM: Piecewise structural equation modeling in R for ecology, evolution, and systematics. Methods Ecol. Evol. 7, 573–579 (2016).

    Article  Google Scholar 

  76. R Core Team R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2020); https://www.R-project.org/

Download references

Acknowledgements

We thank M. C. Hutchinson, A. P. A. Assis, G. Burin, J. Diez, J. Gillung, P. R. Guimarães Jr and B. B. Mora for their thoughtful discussions and comments on the manuscript, J. Lefcheck for his assistance with the structural equation models and A. R. Cirtwill for discussions regarding motif analysis. We also thank the growers and landowners that allowed us to work on their property and greatly appreciate the identification assistance of expert taxonomists J. Gibbs, M. Hauser, J. Pawelek and the late R. Thorp. This work was supported by funding from the Army Research Office (W911NF-11-1-0361 to C.K.), the Natural Resources Conservation Service (CIG-69-3A75-12-253, CIG-69-3A75-9-142, CIG-68-9104-6-101 and WLF-69-7482-6-277 to the Xerces Society), the National Science Foundation (DEB-0919128 to C.K.), The US Department of Agriculture (USDA-NIFA 2012-51181-20105 to Michigan State University) and a USDA NIFA fellowship to L.C.P. M.P.G. acknowledges funding provided by the University of California Chancellor’s Postdoctoral Fellowship from UC Riverside.

Author information

Author notes

  1. Marília Palumbo Gaiarsa

    Present address: Department of Evolutionary Biology and Environmental Studies, University of Zurich, Zurich, Switzerland

Authors and Affiliations

  1. Department of Entomology, University of California, Riverside, CA, USA

    Marília Palumbo Gaiarsa & Lauren C. Ponisio

  2. Department of Environmental Science, Policy, and Management, University of California, Berkeley, CA, USA

    Claire Kremen

  3. Institute for Resources, Environment and Sustainability, Department of Zoology and Biodiversity Research Centre, University of British Columbia, Vancouver, British Columbia, Canada

    Claire Kremen

  4. Institute of Ecology and Evolution, Department of Biology, University of Oregon, Eugene, OR, USA

    Lauren C. Ponisio

Authors
  1. Marília Palumbo Gaiarsa
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Claire Kremen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Lauren C. Ponisio
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

M.P.G. and L.C.P. designed the analysis. C.K. designed the field study. L.C.P. and C.K. collected data. M.P.G. and L.C.P. developed the metrics for interaction flexibility, which M.P.G. implemented. L.C.P. wrote the first version of the occupancy models, which M.P.G. modified and refined for this study. M.P.G. wrote the manuscript, performed analyses and prepared the figures. All authors contributed to revisions.

Corresponding author

Correspondence to Marília Palumbo Gaiarsa.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Peer review information Nature Ecology & Evolution thanks Gita Benadi and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Supplementary Information

Supplementary Figs. 1–4, Discussion and Tables 1–6.

Reporting Summary

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gaiarsa, M.P., Kremen, C. & Ponisio, L.C. Pollinator interaction flexibility across scales affects patch colonization and occupancy. Nat Ecol Evol 5, 787–793 (2021). https://doi.org/10.1038/s41559-021-01434-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41559-021-01434-y

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing