Abstract
Quantifying changes in functional diversity, the facet of biodiversity accounting for the biological features of organisms, has been advocated as one of the most integrative ways to unravel how communities are affected by human-induced perturbations. The present study assessed how functional diversity patterns varied among communities that differed in the degree to which non-native species dominated the community in temperate lake fish communities and whether accounting for intraspecific functional variability could provide a better understanding of the variation of functional diversity across communities. Four functional diversity indices were computed for 18 temperate lake fish communities along a gradient of non-native fish dominance using morphological functional traits assessed for each life-stage within each species. First, we showed that intraspecific variability in functional traits was high and comparable to interspecific variability. Second, we found that non-native fish were functionally distinct from native fish. Finally, we demonstrated that there was a significant relationship between functional diversity and the degree to which non-native fish currently dominated the community and that this association could be better detected when accounting for intraspecific functional variability. These findings highlighted the importance of incorporating intraspecific variability to better quantify the variation of functional diversity patterns in communities facing human-induced perturbations.
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Adler PB, Fajardo A, Kleinhesselink AR, Kraft NJB (2013) Trait-based tests of coexistence mechanisms. Ecol Lett 16:1294–1306. https://doi.org/10.1111/ele.12157
Albert CH, de Bello F, Boulangeat I et al (2012) On the importance of intraspecific variability for the quantification of functional diversity. Oikos 121:116–126. https://doi.org/10.1111/j.1600-0706.2011.19672.x
Albouy C, Guilhaumon F, Villéger S et al (2011) Predicting trophic guild and diet overlap from functional traits: statistics, opportunities and limitations for marine ecology. Mar Ecol Prog Ser 436:17–28. https://doi.org/10.3354/meps09240
Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46. https://doi.org/10.1111/j.1442-9993.2001.01070.pp.x
Anderson CB, Rosemond AD (2007) Ecosystem engineering by invasive exotic beavers reduces in-stream diversity and enhances ecosystem function in Cape Horn, Chile. Oecologia 154:141–153. https://doi.org/10.1007/s00442-007-0757-4
Azzurro E, Tuset VM, Lombarte A et al (2014) External morphology explains the success of biological invasions. Ecol Lett 17:1455–1463. https://doi.org/10.1111/ele.12351
Bellwood D, Wainwright P, Fulton C, Hoey A (2006) Functional versatility supports coral reef biodiversity. Proc R Soc B Biol Sci 273:101–107. https://doi.org/10.1098/rspb.2005.3276
Blanchet S, Grenouillet G, Beauchard O et al (2010) Non-native species disrupt the worldwide patterns of freshwater fish body size: implications for Bergmann’s rule. Ecol Lett 13:421–431. https://doi.org/10.1111/j.1461-0248.2009.01432.x
Bolnick DI, Amarasekare P, Araújo MS et al (2011) Why intraspecific trait variation matters in community ecology. Trends Ecol Evol 26:183–192. https://doi.org/10.1016/j.tree.2011.01.009
Buckley YM, Catford J (2016) Does the biogeographic origin of species matter? Ecological effects of native and non-native species and the use of origin to guide management. J Ecol 104:4–17. https://doi.org/10.1111/1365-2745.12501
Carol J, Zamora L, García-Berthou E (2007) Preliminary telemetry data on the movement patterns and habitat use of European catfish (Silurus glanis) in a reservoir of the River Ebro, Spain. Ecol Freshw Fish 16:450–456. https://doi.org/10.1111/j.1600-0633.2007.00225.x
Cianciaruso MV, Batalha MA, Gaston KJ, Petchey OL (2009) Including intraspecific variability in functional diversity. Ecology 90:81–89. https://doi.org/10.1890/07-1864.1
Copp GH, Robert Britton J, Cucherousset J et al (2009) Voracious invader or benign feline? A review of the environmental biology of European catfish Silurus glanis in its native and introduced ranges. Fish Fish 10:252–282. https://doi.org/10.1111/j.1467-2979.2008.00321.x
Crawley MJ (2007) The R book. Wiley, New York
Cucherousset J, Blanchet S, Olden JD (2012) Non-native species promote trophic dispersion of food webs. Front Ecol Environ 10:406–408. https://doi.org/10.1890/12.WB.018
Davidson AM, Jennions M, Nicotra AB (2011) Do invasive species show higher phenotypic plasticity than native species and if so, is it adaptive? A meta-analysis: invasive species have higher phenotypic plasticity. Ecol Lett 14:419–431. https://doi.org/10.1111/j.1461-0248.2011.01596.x
de Bello F, Lavorel S, Albert CH et al (2011) Quantifying the relevance of intraspecific trait variability for functional diversity. Methods Ecol Evol 2:163–174. https://doi.org/10.1111/j.2041-210X.2010.00071.x
Des Roches S, Post DM, Turley NE et al (2018) The ecological importance of intraspecific variation. Nat Ecol Evol 2:57–64. https://doi.org/10.1038/s41559-017-0402-5
Díaz S, Purvis A, Cornelissen JHC et al (2013) Functional traits, the phylogeny of function, and ecosystem service vulnerability. Ecol Evol 3:2958–2975. https://doi.org/10.1002/ece3.601
Didham RK, Tylianakis JM, Hutchison MA et al (2005) Are invasive species the drivers of ecological change? Trends Ecol Evol 20:470–474. https://doi.org/10.1016/j.tree.2005.07.006
Elleouet J, Albouy C, Ben Rais Lasram F et al (2014) A trait-based approach for assessing and mapping niche overlap between native and exotic species: the Mediterranean coastal fish fauna as a case study. Divers Distrib 20:1333–1344. https://doi.org/10.1111/ddi.12235
Evangelista C, Lecerf A, Britton JR, Cucherousset J (2017) Resource composition mediates the effects of intraspecific variability in nutrient recycling on ecosystem processes. Oikos. https://doi.org/10.1111/oik.03787
Evans KL, Jackson SF, Greenwood JJ, Gaston KJ (2006) Species traits and the form of individual species-energy relationships. Proc R Soc B Biol Sci 273:1779–1787. https://doi.org/10.1098/rspb.2006.3487
Froese R, Pauly D (2014) World Wide Web electronic publication. http://www.fishbase.org, version (last accessed 29/10/2014)
Gagic V, Bartomeus I, Jonsson T et al (2015) Functional identity and diversity of animals predict ecosystem functioning better than species-based indices. Proc R Soc B Biol Sci 282:20142620–20142620. https://doi.org/10.1098/rspb.2014.2620
Gaston KJ (1996) Biodiversity: a biology of numbers and difference. Blackwell, Oxford
Gerisch M, Agostinelli V, Henle K, Dziock F (2012) More species, but all do the same: contrasting effects of flood disturbance on ground beetle functional and species diversity. Oikos 121:508–515. https://doi.org/10.1111/j.1600-0706.2011.19749.x
Gibson PP, Olden JD, O’Neill MW (2015) Beaver dams shift desert fish assemblages toward dominance by non-native species (Verde River, Arizona, USA). Ecol Freshw Fish 24:355–372. https://doi.org/10.1111/eff.12150
González-Suárez M, Bacher S, Jeschke JM (2015) Intraspecific trait variation is correlated with establishment success of alien mammals. Am Nat 185:737–746. https://doi.org/10.1086/681105
Heard MJ, Sax DF (2013) Coexistence between native and exotic species is facilitated by asymmetries in competitive ability and susceptibility to herbivores. Ecol Lett 16:206–213. https://doi.org/10.1111/ele.12030
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
Jeschke JM, Strayer DL (2006) Determinants of vertebrate invasion success in Europe and North America. Glob Change Biol 12:1608–1619. https://doi.org/10.1111/j.1365-2486.2006.01213.x
Juette T, Cucherousset J, Cote J (2014) Animal personality and the ecological impacts of freshwater non-native species. Curr Zool 60:417–427
Jung V, Violle C, Mondy C et al (2010) Intraspecific variability and trait-based community assembly: intraspecific variability and community assembly. J Ecol 98:1134–1140. https://doi.org/10.1111/j.1365-2745.2010.01687.x
Kahn RG, Pearson DE, Dick EJ (2004) Comparison of standard length, fork length, and total length for measuring west coast marine fishes. Mar Fish Rev 66:31–33
Karpouzi VS, Stergiou KI (2003) The relationships between mouth size and shape and body length for 18 species of marine fishes and their trophic implications. J Fish Biol 62:1353–1365. https://doi.org/10.1046/j.1095-8649.2003.00118.x
Kaspari M (2001) Taxonomic level, trophic biology and the regulation of local abundance. Glob Ecol Biogeogr 10:229–244. https://doi.org/10.1046/j.1466-822X.2001.00214.x
Keith P, Persat H, Feunteun E, Allardi J (2011) Les poissons d’eau douce de France. Publication scientifique du Museum, Biotope Editions, Paris
Kraft NJB, Valencia R, Ackerly DD (2008) Functional traits and niche-based tree community assembly in an Amazonian forest. Science 322:580–582. https://doi.org/10.1126/science.1160662
Kraft NJB, Godoy O, Levine JM (2015) Plant functional traits and the multidimensional nature of species coexistence. Proc Natl Acad Sci 112:797–802. https://doi.org/10.1073/pnas.1413650112
Laforest-Lapointe I, Martínez-Vilalta J, Retana J (2014) Intraspecific variability in functional traits matters: case study of Scots pine. Oecologia 175:1337–1348. https://doi.org/10.1007/s00442-014-2967-x
Lefcheck JS, Duffy JE (2015) Multitrophic functional diversity predicts ecosystem functioning in experimental assemblages of estuarine consumers. Ecology 96:2973–2983. https://doi.org/10.1890/14-1977.1
Macarthur R, Levins R (1967) The limiting similarity, convergence, and divergence of coexisting species. Am Nat 101:377–385. https://doi.org/10.1086/282505
Maire E, Grenouillet G, Brosse S, Villéger S (2015) How many dimensions are needed to accurately assess functional diversity? A pragmatic approach for assessing the quality of functional spaces. Glob Ecol Biogeogr 24:728–740. https://doi.org/10.1111/geb.12299
Mason NWH, Irz P, Lanoiselée C et al (2008) Evidence that niche specialization explains species–energy relationships in lake fish communities. J Anim Ecol 77:285–296. https://doi.org/10.1111/j.1365-2656.2007.01350.x
Mitchell RM, Bakker JD (2014) Quantifying and comparing intraspecific functional trait variability: a case study with Hypochaeris radicata. Funct Ecol 28:258–269. https://doi.org/10.1111/1365-2435.12167
Mouillot D, Graham NAJ, Villéger S et al (2013) A functional approach reveals community responses to disturbances. Trends Ecol Evol 28:167–177. https://doi.org/10.1016/j.tree.2012.10.004
Olden JD, Poff NL, Bestgen KR (2006) Life-history strategies predict fish invasions and extirpations in the Colorado river basin. Ecol Monogr 76:25–40. https://doi.org/10.1890/05-0330
Ordonez A, Wright IJ, Olff H (2010) Functional differences between native and alien species: a global-scale comparison: functional differences of native and alien plants. Funct Ecol 24:1353–1361. https://doi.org/10.1111/j.1365-2435.2010.01739.x
Pool TK, Olden JD, Whittier JB, Paukert CP (2010) Environmental drivers of fish functional diversity and composition in the Lower Colorado River Basin. Can J Fish Aquat Sci 67:1791–1807. https://doi.org/10.1139/F10-095
R development core team (2011) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/. Accessed 12 Nov 2018
Raffard A, Santoul F, Cucherousset J, Blanchet S (2018) The community and ecosystem consequences of intraspecific diversity: a meta-analysis. Biol Rev. https://doi.org/10.1111/brv.12472 (in press)
Richards CL, Bossdorf O, Muth NZ et al (2006) Jack of all trades, master of some? On the role of phenotypic plasticity in plant invasions. Ecol Lett 9:981–993. https://doi.org/10.1111/j.1461-0248.2006.00950.x
Roxburgh SH, Shea K, Wilson JB (2004) The intermediate disturbance hypothesis: patch dynamics and mechanisms of species coexistence. Ecology 85:359–371. https://doi.org/10.1890/03-0266
Rudolf VHW (2012) Seasonal shifts in predator body size diversity and trophic interactions in size-structured predator-prey systems. J Anim Ecol 81:524–532. https://doi.org/10.1111/j.1365-2656.2011.01935.x
Rudolf VHW, Lafferty KD (2011) Stage structure alters how complexity affects stability of ecological networks. Ecol Lett 14:75–79. https://doi.org/10.1111/j.1461-0248.2010.01558.x
Rudolf VHW, Rasmussen NL (2013a) Ontogenetic functional diversity: size structure of a keystone predator drives functioning of a complex ecosystem. Ecology 94:1046–1056. https://doi.org/10.1890/12-0378.1
Rudolf VHW, Rasmussen NL (2013b) Population structure determines functional differences among species and ecosystem processes. Nat Commun 4:2318. https://doi.org/10.1038/ncomms3318
Rudolf VHW, Van Allen BG (2017) Legacy effects of developmental stages determine the functional role of predators. Nat Ecol Evol 1:0038. https://doi.org/10.1038/s41559-016-0038
Rudolf VHW, Rasmussen NL, Dibble CJ, Van Allen BG (2014) Resolving the roles of body size and species identity in driving functional diversity. Proc R Soc B Biol Sci 281:20133203–20133203. https://doi.org/10.1098/rspb.2013.3203
Shea K, Roxburgh SH, Rauschert ESJ (2004) Moving from pattern to process: coexistence mechanisms under intermediate disturbance regimes. Ecol Lett 7:491–508. https://doi.org/10.1111/j.1461-0248.2004.00600.x
Simberloff D, Martin J-L, Genovesi P et al (2013) Impacts of biological invasions: what’s what and the way forward. Trends Ecol Evol 28:58–66. https://doi.org/10.1016/j.tree.2012.07.013
Stachowicz JJ, Tilman D (2005) Species invasions and the relationships between species diversity, community saturation, and ecosystem functioning. In: Sax DF, Stachowicz JJ, Gaines SD (eds) Species invasions: insights into ecology, evolution, and biogeography. Sinauer, Sunderland, pp 41–64
Stohlgren TJ, Binkley D, Chong GW et al (1999) Exotic plant species invade hot spots of native plant diversity. Ecol Monogr 69:25–46. https://doi.org/10.1890/0012-9615(1999)069%5b0025:EPSIHS%5d2.0.CO;2
Taudiere A, Violle C (2016) Cati: an R package using functional traits to detect and quantify multi-level community assembly processes. Ecography 39:699–708. https://doi.org/10.1111/ecog.01433
Tedesco PA, Ibañez C, Moya N et al (2007) Local-scale species–energy relationships in fish assemblages of some forested streams of the Bolivian Amazon. C R Biol 330:255–264. https://doi.org/10.1016/j.crvi.2007.02.004
Tilman D (1997) Community invasibility, recruitment limitation, and grassland biodiversity. Ecology 78:81–92. https://doi.org/10.1890/0012-9658(1997)078%5b0081:CIRLAG%5d2.0.CO;2
Turgeon K, Solomon CT, Nozais C, Gregory-Eaves I (2016) Do novel ecosystems follow predictable trajectories? Testing the trophic surge hypothesis in reservoirs using fish. Ecosphere 7:e01617. https://doi.org/10.1002/ecs2.1617
van Kleunen M, Weber E, Fischer M (2010) A meta-analysis of trait differences between invasive and non-invasive plant species. Ecol Lett 13:235–245. https://doi.org/10.1111/j.1461-0248.2009.01418.x
Villéger S, Mason NWH, Mouillot D (2008) New multidimensional functional diversity indices for a multifaceted framework in functional ecology. Ecology 89:2290–2301. https://doi.org/10.1890/07-1206.1
Villéger S, Miranda JR, Hernández DF, Mouillot D (2010) Contrasting changes in taxonomic vs. functional diversity of tropical fish communities after habitat degradation. Ecol Appl 20:1512–1522. https://doi.org/10.1890/09-1310.1
Villéger S, Grenouillet G, Brosse S (2013) Decomposing functional β-diversity reveals that low functional β-diversity is driven by low functional turnover in European fish assemblages. Glob Ecol Biogeogr 22:671–681. https://doi.org/10.1111/geb.12021
Villéger S, Grenouillet G, Brosse S (2014) Functional homogenization exceeds taxonomic homogenization among European fish assemblages. Glob Ecol Biogeogr 23:1450–1460. https://doi.org/10.1111/geb.12226
Villéger S, Brosse S, Mouchet M et al (2017) Functional ecology of fish: current approaches and future challenges. Aquat Sci. https://doi.org/10.1007/s00027-017-0546-z
Violle C, Navas M-L, Vile D et al (2007) Let the concept of trait be functional! Oikos 116:882–892. https://doi.org/10.1111/j.2007.0030-1299.15559.x
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, Loope LL, Westbrooks R (1996) Biological invasions as global environmental change. Am Sci 84:468–478
Wilcove DS, Rothstein D, Dubow J et al (1998) Quantifying threats to imperiled species in the United States. Bioscience 48:607–615. https://doi.org/10.2307/1313420
Závorka L, Buoro M, Cucherousset J (2018) The negative ecological impacts of a globally introduced species decrease with time since introduction. Glob Change Biol 24:4428–4437. https://doi.org/10.1111/gcb.14323
Zhao T, Villéger S, Lek S, Cucherousset J (2014) High intraspecific variability in the functional niche of a predator is associated with ontogenetic shift and individual specialization. Ecol Evol 4:4649–4657. https://doi.org/10.1002/ece3.1260
Zhao T, Grenouillet G, Pool T et al (2016) Environmental determinants of fish community structure in gravel pit lakes. Ecol Freshw Fish 25:412–421. https://doi.org/10.1111/eff.12222
Acknowledgements
We are grateful to the lake owners and managers for access to the gravel pit lakes and to the gravière team for the help during the fieldwork. We thank L. Comte, T. Pool, the Handling Editor and two anonymous reviewers for their helpful suggestions that improve this manuscript. Fish sampling was performed under the authorizations ‘Arrete Prefectoral 31/07/2012′ and ‘Arrete Prefectoral 10/07/2013′. This work was supported by the ONEMA (Projects ISOLAC and ERADINVA), an ‘‘ERG Marie Curie’’ Grant (PERG08-GA-2010- 276969) to JC and a CSC (China Scholarship Council) scholarship to ZT.
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JC, SV and ZT designed the study. TZ acquired and analyzed the data, wrote the first draft of the manuscript. All authors originally formulated the idea, developed the methodology, and contributed to revisions.
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Zhao, T., Villéger, S. & Cucherousset, J. Accounting for intraspecific diversity when examining relationships between non-native species and functional diversity. Oecologia 189, 171–183 (2019). https://doi.org/10.1007/s00442-018-4311-3
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DOI: https://doi.org/10.1007/s00442-018-4311-3