Abstract
As local communities within a metacommunity may differ considerably in their contributions to biodiversity and ecosystem functioning, it has been suggested that conservation priority should be given to disproportionately important local communities (i.e., keystone communities). However, we know little about what characterizes a keystone community. Using laboratory protist microcosms as the model system, we examined how the environmental uniqueness and location of a local community affect its contributions to the metacommunities. We found that the removal of local communities with unique environmental conditions, which supported endemic species, reduced regional-scale diversity, qualifying them as regional-scale keystone communities. In addition, the local communities possessing unique environmental conditions had greater impacts on ecosystem functions, including biovolume production and particulate organic matter decomposition. We also found that keystone communities for biovolume production were not keystone for organic matter decomposition, and vice versa. Our study, therefore, demonstrates the important role of keystone communities in maintaining biodiversity and functioning of metacommunities.
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Data will be available from the Dryad Digital Repository if our manuscript is accepted.
References
Altermatt F, Holyoak M (2012) Spatial clustering of habitat structure effects patterns of community composition and diversity. Ecology 93:1125–1133. https://doi.org/10.1890/11-1190.1
Brooks TM, Mittermeier RA, Da Fonseca GAB et al (2006) Global biodiversity conservation priorities. Science 313:58–61. https://doi.org/10.1126/science.1127609
Brose U (2003a) Bottom-up control of carabid beetle communities in early successional wetlands: mediated by vegetation structure or plant diversity? Oecologia 135:407–413. https://doi.org/10.1007/s00442-003-1222-7
Brose U (2003b) Regional diversity of temporary wetland carabid beetle communities: a matter of landscape features or cultivation intensity? Agric Ecosyst Environ 98:163–167. https://doi.org/10.1016/S0167-8809(03)00078-1
Cadotte MW (2006) Dispersal and species diversity: a meta-analysis. Am Nat 167:913–924. https://doi.org/10.1086/504850
Cadotte MW, Fukami T (2005) Dispersal, spatial scale, and species diversity in a hierarchically structured experimental landscape. Ecol Lett 8:548–557. https://doi.org/10.1111/j.1461-0248.2005.00750.x
Cardinale BJ, Srivastava DS, Emmett Duffy J et al (2006) Effects of biodiversity on the functioning of trophic groups and ecosystems. Nature 443:989–992. https://doi.org/10.1038/nature05202
Cardinale BJ, Duffy JE, Gonzalez A et al (2012) Biodiversity loss and its impacton humanity. Nature 489:59–67. https://doi.org/10.1038/nature11148
Carrara F, Altermatt F, Rodriguez-Iturbe I, Rinaldo A (2012) Dendritic connectivity controls biodiversity patterns in experimental metacommunities. Proc Natl Acad Sci U S A 109:5761–5766. https://doi.org/10.1073/pnas.1119651109
Carrara F, Rinaldo A, Giometto A, Altermatt F (2014) Complex interaction of dendritic connectivity and hierarchical patch size on biodiversity in river-like landscapes. Am Nat 183:13–25. https://doi.org/10.1086/674009
Chase JM, Leibold MA (2003) Ecological niches: linking classical and contemporary approaches. University of Chicago Press, Chicago
Davidar P, Yoganand K, Ganesh T (2001) Distribution of forest birds in the Andaman islands: Importance of key habitats. J Biogeogr 28:663–671. https://doi.org/10.1046/j.1365-2699.2001.00584.x
Dirzo R, Raven PH (2003) Global state of biodiversity and loss. Annu Rev Environ Resour 28:137–167. https://doi.org/10.1146/annurev.energy.28.050302.105532
Economo EP (2011) Biodiversity conservation in metacommunity networks: linking pattern and persistence. Am Nat 177:E167–E180. https://doi.org/10.1086/659946
Fahrig L (2002) Effect of habitat fragmentation on the extinction threshhold: a synthesis. Ecol Appl 12:346–353. https://doi.org/10.1890/1051-0761(2002)012[0346:EOHFOT]2.0.CO;2
Fahrig L (2003) Effects of habitat fragmentation on biodiversity. Annu Rev Ecol Evol Syst 34:487–515. https://doi.org/10.1146/annurev.ecolsys.34.011802.132419
Gascuel F, Laroche F, Bonnet-Lebrun AS, Rodrigues ASL (2016) The effects of archipelago spatial structure on island diversity and endemism: predictions from a spatially-structured neutral model. Evolution (N Y) 70:2657–2666. https://doi.org/10.1111/evo.13067
Gonzalez A, Mouquet N, Loreau M (2009) Biodiversity as spatial insurance: the effects of habitat fragmentation and dispersal on ecosystem functioning. In: Naeem S, Bunker DE, Hector A, et al. (eds) Biodiversity, ecosystem functioning, and human wellbeing: an ecological and economic perspective. Oxford University Press, Oxford
Gounand I, Harvey E, Ganesanandamoorthy P, Altermatt F (2017) Subsidies mediate interactions between communities across space. Oikos 126:972–979. https://doi.org/10.1111/oik.03922
Grace JB, Anderson TM, Seabloom EW et al (2016) Integrative modelling reveals mechanisms linking productivity and plant species richness. Nature 529:390–393. https://doi.org/10.1038/nature16524
Gravel D, Guichard F, Loreau M, Mouquet N (2010) Source and sink dynamics in meta-ecosystems. Ecology 91:2172–2184. https://doi.org/10.1890/09-0843.1
Gu F, Chen L, Ni B, Zhang X (2002) A comparative study on the electron microscopic enzymo-cytochemistry of Paramecium bursaria from light and dark cultures. Eur J Protistol 38:267–278. https://doi.org/10.1078/0932-4739-00875
Haddad NM, Brudvig LA, Clobert J et al (2015) Habitat fragmentation and its lasting impact on Earth’s ecosystems. Sci Adv 1:1–9. https://doi.org/10.1126/sciadv.1500052
Holyoak M, Leibold MA, Holt RD (2005) Meta-communities: spatial dynamics and ecological communities. University of Chicago Press, USA
Hooper DU, Chapin FS, Ewel JJ et al (2005) Effects of biodiversity on ecosystem functioning: a consensus of current knowledge. Ecol Monogr 75:3–35. https://doi.org/10.1890/04-0922
Hooper DU, Adair EC, Cardinale BJ et al (2012) A global synthesis reveals biodiversity loss as a major driver of ecosystem change. Nature 486:105–108. https://doi.org/10.1038/nature11118
Jackson ST, Sax DF (2010) Balancing biodiversity in a changing environment: extinction debt, immigration credit and species turnover. Trends Ecol Evol 25:153–160
Legendre P, De Cáceres M (2013) Beta diversity as the variance of community data: dissimilarity coefficients and partitioning. Ecol Lett 16:951–963. https://doi.org/10.1111/ele.12141
Leibold MA (1998) Similarity and local co-existence of species in regional biotas. Evol Ecol 12:95–110. https://doi.org/10.1023/A:1006511124428
Leibold MA, Holyoak M, Mouquet N et al (2004) The metacommunity concept: a framework for multi-scale community ecology. Ecol Lett 7:601–613. https://doi.org/10.1111/j.1461-0248.2004.00608.x
Loreau M, Mouquet N (1999) Immigration and the maintenance of local species diversity. Am Nat 154:427–440. https://doi.org/10.1086/303252
Loreau M, Mouquet N, Gonzalez A (2003a) Biodiversity as spatial insurance in heterogeneous landscapes. Proc Natl Acad Sci 100:12765–12770. https://doi.org/10.1073/pnas.2235465100
Loreau M, Mouquet N, Holt RD (2003b) Meta-ecosystems: a theoretical framework for a spatial ecosystem ecology. Ecol Lett 6:673–679. https://doi.org/10.1046/j.1461-0248.2003.00483.x
Michels E, Cottenie K, Neys L, De Meester L (2001) Zooplankton on the move: first results on the quantification of dispersal of zooplankton in a set of interconnected ponds. Hydrobiologia 442:117–126. https://doi.org/10.1023/A:1017549416362
Mills LS, Soulé ME, Doak DF (1993) The keystone-species concept in ecology and conservation: management and policy must explicitly consider the complexity of interactions in natural systems. Bioscience 43:219–224. https://doi.org/10.1038/23631
Mouquet N, Loreau M (2002) Coexistence in metacommunities: the regional similarity hypothesis. Am Nat 159:420–426. https://doi.org/10.1086/338996
Mouquet N, Loreau M (2003) Community patterns in source-sink metacommunities. Am Nat 162:544–557. https://doi.org/10.1007/s11172-006-0459-9
Mouquet N, Miller TE, Daufresne T, Kneitel JM (2006) Consequences of varying regional heterogeneity in source-sink metacommunities. Oikos 113:481–488. https://doi.org/10.1111/j.2006.0030-1299.14582.x
Mouquet N, Gravel D, Massol F, Calcagno V (2013) Extending the concept of keystone species to communities and ecosystems. Ecol Lett 16:1–8. https://doi.org/10.1111/ele.12014
Muneepeerakul R, Bertuzzo E, Lynch HJ et al (2008) Neutral metacommunity models predict fish diversity patterns in Mississippi–Missouri basin. Nature 453:220–222. https://doi.org/10.1038/nature06813
Myers N, Mittermeler RA, Mittermeler CG et al (2000) Biodiversity hotspots for conservation priorities. Nature 403:853–858. https://doi.org/10.1038/35002501
Naeem S, Duffy JE, Zavaleta E (2012) The functions of biological diversity in an age of extinction. Science 336:1401–1406. https://doi.org/10.1126/science.1215855
Paine RT (1966) Food web complexity and species diversity. Am Nat 100:65–75. https://doi.org/10.1086/282400
Paine RT (1969) A note on trophic complexity and community stability. Am Nat 103:91–93. https://doi.org/10.1086/282586
Palmer MA, Zedler JB, Falk DA (2016) Ecological theory and restoration ecology. Foundations of restoration ecology. Island Press/Center for Resource Economics, Washington, pp 3–26
Pimm SL, Jenkins CN, Abell R et al (2014) The biodiversity of species and their rates of extinction, distribution, and protection. Science 344:1246752. https://doi.org/10.1126/science.1246752
Polis GA, Anderson WB, Holt RD (1997) Toward an integration of landscape and food web ecology: the dynamics of spatially subsidized food webs. Annu Rev Ecol Syst 28:289–316. https://doi.org/10.1146/annurev.ecolsys.28.1.289
Power ME, Tilman D, Estes JA et al (1996) Challenges in the quest for keystones. Bioscience 46:609–620. https://doi.org/10.2307/1312990
Pulliam HR (1988) Sources, sinks, and population regulation. Am Nat 132:652–661. https://doi.org/10.1086/284880
R core team (2017) R: a language and environment for statistical computing. R Found Stat Comput Vienna, Austria. https://www.R-project.org/
Resetarits EJ, Cathey SE, Leibold MA (2018) Testing the keystone community concept: effects of landscape, patch removal, and environment on metacommunity structure. Ecology 99:57–67. https://doi.org/10.1002/ecy.2041
Rey Benayas JM, Newton AC, Diaz A, Bullock JM (2009) Enhancement of biodiversity and ecosystem services by ecological restoration: a meta-analysis. Science 325:1121–1124. https://doi.org/10.1126/science.1172460
Saura S, Bodin Ö, Fortin MJ (2014) Step** stones are crucial for species’ long-distance dispersal and range expansion through habitat networks. J Appl Ecol 51:171–182. https://doi.org/10.1111/1365-2664.12179
Shanafelt DW, Dieckmann U, Jonas M et al (2015) Biodiversity, productivity, and the spatial insurance hypothesis revisited. J Theor Biol 380:426–435. https://doi.org/10.1016/j.jtbi.2015.06.017
Staddon P, Lindo Z, Crittenden PD et al (2010) Connectivity, non-random extinction and ecosystem function in experimental metacommunities. Ecol Lett 13:543–552. https://doi.org/10.1111/j.1461-0248.2010.01450.x
Tews J, Brose U, Grimm V et al (2004) Animal species diversity driven by habitat heterogeneity/diversity: the importance of keystone structures. J Biogeogr 31:79–92. https://doi.org/10.1046/j.0305-0270.2003.00994.x
Thompson PL, Rayfield B, Gonzalez A (2017) Loss of habitat and connectivity erodes species diversity, ecosystem functioning, and stability in metacommunity networks. Ecography (Cop) 40:98–108. https://doi.org/10.1111/ecog.02558
Tilman D, May RM, Lehman CL, Nowak MA (1994) Habitat destruction and the extinction debt. Nature 371:65–66. https://doi.org/10.1038/371065a0
Venail PA, Maclean RC, Meynard CN, Mouquet N (2010) Dispersal scales up the biodiversity-productivity relationship in an experimental source-sink metacommunity. Proc R Soc B Biol Sci 277:2339–2345. https://doi.org/10.1098/rspb.2009.2104
Violle C, Enquist BJ, McGill BJ et al (2012) The return of the variance: intraspecific variability in community ecology. Trends Ecol Evol 27:244–252. https://doi.org/10.1016/J.TREE.2011.11.014
Vitousek PM, Mooney HA, Lubchenco J, Melillo JM, Vitousek PM, Mooney HA, Lubchenco JMJ (1997) Human domination of Earth’s ecosystems. Science 277:494–499. https://doi.org/10.1126/science.277.5325.494
Wetzel RG, Likens GE (2000) Limnological analyses, 3rd edn. Springer, New York
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This project was supported by the National Science Foundation of USA (Grant No. DEB‐1342754, DEB‐1856318 and CBET‐1833988).
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XY and JT conceived and designed the experiments. XY, JT, and KHS performed the experiments. XY analyzed the data. XY, JT, and LJ wrote the manuscript.
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Communicated by Jamie M. Kneitel.
Our study provides empirical evidence of keystone communities. Using laboratory protist communities as model systems, we show that the loss of keystone communities carries significant consequence for biodiversity and ecosystem functioning at both local and regional scales. Our findings have important implications for the effective allocation of conservation resources.
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Yang, X., Tan, J., Sun, K.H. et al. Experimental demonstration of the importance of keystone communities for maintaining metacommunity biodiversity and ecosystem functioning. Oecologia 193, 437–447 (2020). https://doi.org/10.1007/s00442-020-04693-x
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DOI: https://doi.org/10.1007/s00442-020-04693-x