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.
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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).
Tews, J. et al. Animal species diversity driven by habitat heterogeneity/diversity: the importance of keystone structures. J. Biogeogr. 31, 79–92 (2004).
Bruno, J. F., Stachowicz, J. J. & Bertness, M. D. Inclusion of facilitation into ecological theory. Trends Ecol. Evol. 18, 119–125 (2003).
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).
Jones, C. G., Lawton, J. H. & Shachak, M. Organisms as ecosystem engineers. Oikos 69, 373–386 (1994).
Byers, J. et al. Using ecosystem engineers to restore ecological systems. Trends Ecol. Evol. 21, 493–500 (2006).
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).
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).
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).
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).
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).
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).
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).
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).
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).
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).
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).
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).
Albrecht, A. & Reise, K. Effects of Fucus vesiculosus covering intertidal mussel beds in the Wadden Sea. Helgoländer Meeresunters 48, 243–256 (1994).
Ellwood, M. D. F. & Foster, W. A. Doubling the estimate of invertebrate biomass in a rainforest canopy. Nature 429, 549–551 (2004).
Thomsen, M. S. et al. A sixth-level habitat cascade increases biodiversity in an intertidal estuary. Ecol. Evol 6, 8291–8303 (2016).
Watson, D. M. & Herring, M. Mistletoe as a keystone resource: an experimental test. Proc. R. Soc. B 279, 3853–3860 (2012).
Borer, E. T. et al. What determines the strength of a trophic cascade? Ecology 86, 528–537 (2005).
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).
Shurin, J. B. et al. A cross‐ecosystem comparison of the strength of trophic cascades. Ecol. Lett. 5, 785–791 (2002).
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).
Koricheva, J, . & Gurevitch, J. & Mengersen, K. Handbook of Meta-analysis in Ecology and Evolution. (Princeton Univ. Press: Princeton, 2013).
McIntire, E. J. & Fajardo, A. Facilitation as a ubiquitous driver of biodiversity. New Phytol. 201, 403–416 (2014).
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).
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).
Armbruster, P., Hutchinson, R. A. & Cotgreave, P. Factors influencing community structure in a South American tank bromeliad fauna. Oikos 96, 225–234 (2002).
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).
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).
Frankham, R. Relationship of genetic variation to population size in wildlife. Conserv. Biol. 10, 1500–1508 (1996).
Frankham, R. Genetics and extinction. Biol. Conserv. 126, 131–140 (2005).
Angelini, C. & Briggs, K. Spillover of secondary foundation species transforms community structure and accelerates decomposition in oak savannas. Ecosystems 18, 780–791 (2015).
Kéfi, S. et al. Network structure beyond food webs: mapping non-trophic and trophic interactions on Chilean rocky shores. Ecology 96, 291–303 (2015).
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).
Hylander, K. & Nemomissa, S. Home garden coffee as a repository of epiphyte biodiversity in Ethiopia. Front. Ecol. Environ. 6, 524–528 (2008).
Rosenberg, M. S, Adams, D. C. & Gurevitch, J. Metawin: Statistical Software for Meta-analysis, Version 2 128. (Sinauer Associates: Sunderland, MA, 2000).
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).
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).
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).
Viechtbauer, W. Conducting meta-analyses in R with the metafor package. J. Stat. Softw. 36, 1–48 (2010).
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).
Watson, D. M. Effects of mistletoe on diversity: a case-study from southern New South Wales. Emu 102, 275–281 (2002).
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).
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).
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)..
Wahl, M. & Mark, O. The predominantly facultative nature of epibiosis: experimental and observational evidence. Mar. Ecol. Progress Ser. 187, 59–66 (1999).
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’.
The authors declare no competing financial interests.
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Thomsen, M.S., Altieri, A.H., Angelini, C. et al. Secondary foundation species enhance biodiversity. Nat Ecol Evol 2, 634–639 (2018). https://doi.org/10.1038/s41559-018-0487-5
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