Skip to main content

Thank you for visiting 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.

Secondary foundation species enhance biodiversity


It has long been recognized that primary foundation species (FS), such as trees and seagrasses, enhance biodiversity. Among the species facilitated are secondary FS, including mistletoes and epiphytes. Case studies have demonstrated that secondary FS can further modify habitat-associated organisms (‘inhabitants’), but their net effects remain unknown. Here we assess how inhabitants, globally, are affected by secondary FS. We extracted and calculated 2,187 abundance and 397 richness Hedges’ g effect sizes from 91 and 50 publications, respectively. A weighted meta-analysis revealed that secondary FS significantly enhanced the abundance and richness of inhabitants compared to the primary FS alone. This indirect facilitation arising through sequential habitat formation was consistent across environmental and experimental conditions. Complementary unweighted analyses on log response ratios revealed that the magnitude of these effects was similar to the global average strength of direct facilitation from primary foundation species and greater than the average strength of trophic cascades, a widely recognized type of indirect facilitation arising through sequential consumption. The finding that secondary FS enhance the abundance and richness of inhabitants has important implications for understanding the mechanisms that regulate biodiversity. Integrating secondary FS into conservation practice will improve our ability to protect biodiversity and ecosystem function.

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

Relevant articles

Open Access articles citing this article.

Access options

Rent or buy this article

Get just this article for as long as you need it


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

Fig. 1: Primary and secondary foundation species and their inhabitants: definitions and examples.
Fig. 2: Effects of secondary FS on abundance and taxonomic richness of inhabitants.


  1. Romero, G. Q., Gonçalves-Souza, T., Vieira, C. & Koricheva, J. Ecosystem engineering effects on species diversity across ecosystems: a meta-analysis. Biol. Rev. 90, 877–890 (2014).

    Article  Google Scholar 

  2. Tews, J. et al. Animal species diversity driven by habitat heterogeneity/diversity: the importance of keystone structures. J. Biogeogr. 31, 79–92 (2004).

    Article  Google Scholar 

  3. Bruno, J. F., Stachowicz, J. J. & Bertness, M. D. Inclusion of facilitation into ecological theory. Trends Ecol. Evol. 18, 119–125 (2003).

    Article  Google Scholar 

  4. Ellison, A. M. et al. Loss of foundation species: consequences for the structure and dynamics of forested ecosystems. Front. Ecol. Environ. 3, 479–486 (2005).

    Article  Google Scholar 

  5. Jones, C. G., Lawton, J. H. & Shachak, M. Organisms as ecosystem engineers. Oikos 69, 373–386 (1994).

    Article  Google Scholar 

  6. Byers, J. et al. Using ecosystem engineers to restore ecological systems. Trends Ecol. Evol. 21, 493–500 (2006).

    Article  Google Scholar 

  7. Thomsen, M. S. et al. Habitat cascades: the conceptual context and global relevance of facilitation cascades via habitat formation and modification. Integr. Comp. Biol. 50, 158–175 (2010).

    Article  Google Scholar 

  8. Altieri, A. H., Silliman, B. R. & Bertness, M. D. Hierarchical organization via a facilitation cascade in intertidal cordgrass bed communities. Am. Nat. 169, 195–206 (2007).

    Article  Google Scholar 

  9. Mormul, R. P., Thomaz, S. M., da Silveira, M. J. & Rodrigues, L. Epiphyton or macrophyte: which primary producer attracts the snail Hebetancylus moricandi? Am. Malacol. Bull. 28, 127–133 (2010).

    Article  Google Scholar 

  10. Bishop, M. J., Byers, J. E., Marcek, B. J. & Gribben, P. E. Density-dependent facilitation cascades determine epifaunal community structure in temperate Australian mangroves. Ecology 93, 1388–1401 (2012).

    Article  Google Scholar 

  11. Angelini, C. et al. Foundation species' overlap enhances biodiversity and multifunctionality from the patch to landscape scale in southeastern US salt marshes. Proc. R. Soc. B 282, 20150421 (2015).

    Article  Google Scholar 

  12. Thomsen, M. S., Metcalfe, I., South, P. & Schiel, D. R. A host-specific habitat former controls biodiversity across ecological transitions in a rocky intertidal facilitation cascade. Mar. Freshw. Res. 67, 144–152 (2016).

    Article  Google Scholar 

  13. Hughes, A. R., Gribben, P. E., Kimbro, D. L. & Bishop, M. J. Additive and site-specific effects of two foundation species on invertebrate community structure. Mar. Ecol. Progress Ser. 508, 129–138 (2014).

    Article  Google Scholar 

  14. Jaxion-Harm, J. & Speight, M. R. Algal cover in mangroves affects distribution and predation rates by carnivorous fishes. J. Exp. Mar. Biol. Ecol. 414, 19–27 (2012).

    Article  Google Scholar 

  15. Bell, J. D. & Westoby, M. Effects of an epiphytic alga on abundances of fish and decapods associated with the seagrass Zostera capricorni. Aust. J. Ecol. 12, 333–337 (1987).

    Article  Google Scholar 

  16. Bennetts, R. E., White, G. C., Hawksworth, F. G. & Severs, S. E. The influence of dwarf mistletoe on bird communities in Colorado ponderosa pine forests. Ecol. Appl. 6, 899–909 (1996).

    Article  Google Scholar 

  17. Adams, P., Locascio, J. V. & Robbins, B. D. Microhabitat use by a post-settlement stage estuarine fish: evidence from relative abundance and predation among habitats. J. Exp. Mar. Biol. Ecol. 299, 17–33 (2004).

    Article  Google Scholar 

  18. Holmquist, J. G. Disturbance and gap formation in a marine benthic mosaic—influence of shifting macroalgal patches on seagrass structure and mobile invertebrates. Mar. Ecol. Progress Ser. 158, 121–130 (1997).

    Article  Google Scholar 

  19. Albrecht, A. & Reise, K. Effects of Fucus vesiculosus covering intertidal mussel beds in the Wadden Sea. Helgoländer Meeresunters 48, 243–256 (1994).

    Article  Google Scholar 

  20. Ellwood, M. D. F. & Foster, W. A. Doubling the estimate of invertebrate biomass in a rainforest canopy. Nature 429, 549–551 (2004).

    Article  CAS  Google Scholar 

  21. Thomsen, M. S. et al. A sixth-level habitat cascade increases biodiversity in an intertidal estuary. Ecol. Evol 6, 8291–8303 (2016).

    Article  Google Scholar 

  22. Watson, D. M. & Herring, M. Mistletoe as a keystone resource: an experimental test. Proc. R. Soc. B 279, 3853–3860 (2012).

    Article  Google Scholar 

  23. Borer, E. T. et al. What determines the strength of a trophic cascade? Ecology 86, 528–537 (2005).

    Article  Google Scholar 

  24. Schmitz, O. J., Hambäck, P. A. & Beckerman, A. P. Trophic cascades in terrestrial systems: a review of the effects of carnivore removals on plants. Am. Nat. 155, 141–153 (2000).

    Article  Google Scholar 

  25. Shurin, J. B. et al. A cross‐ecosystem comparison of the strength of trophic cascades. Ecol. Lett. 5, 785–791 (2002).

    Article  Google Scholar 

  26. Bruno, J. F. & Bertness, M. D. in Habitat Modification and Facilitation in Benthic Marine Communities (eds Bertness, M. D. et al.) 201–218 (Sinauer Associates, Sunderland, MA, 2001).

  27. Koricheva, J, . & Gurevitch, J. & Mengersen, K. Handbook of Meta-analysis in Ecology and Evolution. (Princeton Univ. Press: Princeton, 2013).

    Book  Google Scholar 

  28. McIntire, E. J. & Fajardo, A. Facilitation as a ubiquitous driver of biodiversity. New Phytol. 201, 403–416 (2014).

    Article  Google Scholar 

  29. Gotelli, N. J. & Colwell, R. K. Quantifying biodiversity: procedures and pitfalls in the measurement and comparison of species richness. Ecol. Lett. 4, 379–391 (2001).

    Article  Google Scholar 

  30. Mellado, A., Morillas, L., Gallardo, A. & Zamora, R. Temporal dynamic of parasite‐mediated linkages between the forest canopy and soil processes and the microbial community. New Phytol. 211, 1382–1392 (2016).

    Article  Google Scholar 

  31. Armbruster, P., Hutchinson, R. A. & Cotgreave, P. Factors influencing community structure in a South American tank bromeliad fauna. Oikos 96, 225–234 (2002).

    Article  Google Scholar 

  32. Balke, M. et al. Ancient associations of aquatic beetles and tank bromeliads in the neotropical forest canopy. Proc. Natl Acad. Sci. USA 105, 6356–6361 (2008).

    Article  CAS  Google Scholar 

  33. Stuntz, S., Linder, C., Linsenmair, K. E., Simon, U. & Zotz, G. Do non-myrmocophilic epiphytes influence community structure of arboreal ants? Basic Appl. Ecol. 4, 363–373 (2003).

    Article  Google Scholar 

  34. Frankham, R. Relationship of genetic variation to population size in wildlife. Conserv. Biol. 10, 1500–1508 (1996).

    Article  Google Scholar 

  35. Frankham, R. Genetics and extinction. Biol. Conserv. 126, 131–140 (2005).

    Article  Google Scholar 

  36. Angelini, C. & Briggs, K. Spillover of secondary foundation species transforms community structure and accelerates decomposition in oak savannas. Ecosystems 18, 780–791 (2015).

    Article  Google Scholar 

  37. Kéfi, S. et al. Network structure beyond food webs: mapping non-trophic and trophic interactions on Chilean rocky shores. Ecology 96, 291–303 (2015).

    Article  Google Scholar 

  38. Silberstein, K., Chiffings, A. & McComb, A. The loss of seagrass in Cockburn Sound, Western Australia. III. The effect of epiphytes on productivity of Posidonia australis Hook. F. Aquat. Bot. 24, 355–371 (1986).

    Article  Google Scholar 

  39. Hylander, K. & Nemomissa, S. Home garden coffee as a repository of epiphyte biodiversity in Ethiopia. Front. Ecol. Environ. 6, 524–528 (2008).

    Article  Google Scholar 

  40. Rosenberg, M. S, Adams, D. C. & Gurevitch, J. Metawin: Statistical Software for Meta-analysis, Version 2 128. (Sinauer Associates: Sunderland, MA, 2000).

    Google Scholar 

  41. Gartner, A., Tuya, F., Lavery, P. S. & McMahon, K. Habitat preferences of macroinvertebrate fauna among seagrasses with varying structural forms. J. Exp. Mar. Biol. Ecol. 439, 143–151 (2013).

    Article  Google Scholar 

  42. Calcagno, V. & de Mazancourt, C. glmulti: an R package for easy automated model selection with (generalized) linear models. J. Stat. Softw. 34, 1–29 (2010).

    Article  Google Scholar 

  43. Rosenberg, M. S. The file-drawer problem revisited: a general weighted method for calculating fail-safe numbers in meta-analysis. Evolution 59, 464–468 (2005).

    Article  Google Scholar 

  44. Viechtbauer, W. Conducting meta-analyses in R with the metafor package. J. Stat. Softw. 36, 1–48 (2010).

    Article  Google Scholar 

  45. Angelini, C., Altieri, A. H., Silliman, B. R. & Bertness, M. D. Interactions among foundation species and their consequences for community organization, biodiversity, and conservation. BioScience 61, 782–789 (2011).

    Article  Google Scholar 

  46. Watson, D. M. Effects of mistletoe on diversity: a case-study from southern New South Wales. Emu 102, 275–281 (2002).

    Article  Google Scholar 

  47. Altieri, A., van Wesenbeeck, B. K., Bertness, M. D. & Silliman, B. R. Facilitation cascade explains positive relationship between native biodiversity and invasion success. Ecology 91, 1269–1275 (2010).

    Article  Google Scholar 

  48. Valentine, J. F. & Heck, K. L. Mussels in seagrass meadows: their influence on macroinvertebrate abundance, and production and macrophyte biomass in the northern Gulf of Mexico. Mar. Ecol. Progress Ser. 96, 63–74 (1993).

    Article  Google Scholar 

  49. Dayton, P. K. Towards an understanding of community resilience and the potential effects of enrichment to the benthos of McMurdo Sound, Antarctica. Proc. Colloquium on Conservation Problems in Antartica 100, 81–96 (1972)..

  50. Wahl, M. & Mark, O. The predominantly facultative nature of epibiosis: experimental and observational evidence. Mar. Ecol. Progress Ser. 187, 59–66 (1999).

    Article  Google Scholar 

Download references


M.S.T. and D.R.S. were supported by the Marsden Fund of the Royal Society of New Zealand and the Coasts and Oceans programme of The National Institute of Water and Atmospheric Research. T.W. and P.E.G. were supported by funding from the Australian Research Council. C.A. was supported by National Science Foundation (NSF) DEB 1546638. P.M.S. is supported by the Cawthron Institute. The authors acknowledge financial support from the Centre of Integrative Ecology, School of Biological Sciences, University of Canterbury, for the workshop ‘Facilitation cascades across ecosystems’.

Author information

Authors and Affiliations



M.S.T. identified relevant literature, extracted all data and calculated effect sizes. M.S.T. and Q.H. analysed the data. All authors contributed to the development of the experimental design, data interpretation and manuscript.

Corresponding author

Correspondence to Mads S. Thomsen.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Additional information

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

Supplementary information

Supplementary Information

Supplementary Methods, Supplementary Figures 1–2, Supplementary References, Supplementary Results.

Life Sciences Reporting Summary

Supplementary Table 1

List of studies and foundation species analysed

Supplementary Data 1

List of all analysed effect sizes and test variables

Rights and permissions

Reprints and Permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Thomsen, M.S., Altieri, A.H., Angelini, C. et al. Secondary foundation species enhance biodiversity. Nat Ecol Evol 2, 634–639 (2018).

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI:

This article is cited by


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