Browse by volume Browse by section Browse by topic Browse by conference

Section: Ecology
Topic: Ecology, Population biology, Statistics

Beyond variance: simple random distributions are not a good proxy for intraspecific variability in systems with environmental structure

Girard-Tercieux, Camille1  ; Vieilledent, Ghislain1 ; Clark, Adam2 ; Clark, James S.3, 4; Courbaud, Benoit4 ; Fortunel, Claire1 ; Kunstler, Georges4 ; Pélissier, Raphaël1 ; Rüger, Nadja5, 6, 7 ; Maréchaux, Isabelle1 
1 AMAP, Université de Montpellier, CIRAD, CNRS, INRAE, IRD, Montpellier, France
2 Institute of Biology, Karl-Franzens University of Graz, Graz, Austria
3 Nicholas School of the Environment, Duke University, Durham (NC), USA
4 Université Grenoble Alpes, INRAE, LESSEM, St. Martin-d’Heres, France
5 Department of Economics, University of Leipzig, Leipzig, Germany
6 German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig, Leipzig, Germany
7 Smithsonian Tropical Research Institute, Balboa, Ancón, Panama

10.24072/pcjournal.360 - Peer Community Journal, Volume 4 (2024), article no. e28.

Get full text PDF Peer reviewed and recommended by PCI

The role of intraspecific variability (IV) in shaping community dynamics and species coexistence has been intensively discussed over the past decade and modelling studies have played an important role in that respect. However, these studies often implicitly assume that IV can be represented by independent random draws around species-specific mean parameters. This major assumption has largely remained undiscussed, although a great part of observed IV is structured in space or time, in particular when environmental dimensions that influence individual performance are imperfectly characterised or unobserved in the field. To test the impact of this strong assumption on the outcome of community dynamics models, we designed a simulation experiment where we varied the level of knowledge of the environment in virtual communities, resulting in different relative importance of explained vs unexplained spatial individual variation in performance. We used a community dynamics simulator to generate communities where the unexplained individual variation is, or is not, added as an unstructured random noise. Communities simulated with unstructured IV never reached the community diversity and composition of those where all the variation was explained and structured (perfect knowledge model). This highlights that incorporating unstructured IV (i.e. a random noise) to account for unexplained (but structured) variation can lead to incorrect simulations of community dynamics. In addition, the effects of unstructured IV on community diversity and composition depended on the relative importance of structured vs unstructured IV, i.e. on the level of knowledge of the environment, which may partly explain the contrasting results of previous studies on the effect of IV on species coexistence. In particular, the effect of unstructured IV on community diversity was positive when the proportion of structured IV vs unstructured IV in the model was low, but negative when this proportion was high. This is because unstructured random noise can either limit the competitive exclusion of inferior competitors in low dimensions or destabilise tight niche partitioning in high dimension. Our study suggests that it is crucial to account for the sources and structure of observed IV in real communities to better understand its effect on community assembly and properly include it in community dynamics models.

Published online:
DOI: 10.24072/pcjournal.360
Type: Research article
Girard-Tercieux, Camille 1; Vieilledent, Ghislain 1; Clark, Adam 2; Clark, James S. 3, 4; Courbaud, Benoit 4; Fortunel, Claire 1; Kunstler, Georges 4; Pélissier, Raphaël 1; Rüger, Nadja 5, 6, 7; Maréchaux, Isabelle 1

1 AMAP, Université de Montpellier, CIRAD, CNRS, INRAE, IRD, Montpellier, France
2 Institute of Biology, Karl-Franzens University of Graz, Graz, Austria
3 Nicholas School of the Environment, Duke University, Durham (NC), USA
4 Université Grenoble Alpes, INRAE, LESSEM, St. Martin-d’Heres, France
5 Department of Economics, University of Leipzig, Leipzig, Germany
6 German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig, Leipzig, Germany
7 Smithsonian Tropical Research Institute, Balboa, Ancón, Panama
License: CC-BY 4.0
Copyrights: The authors retain unrestricted copyrights and publishing rights 
@article{10_24072_pcjournal_360,
     author = {Girard-Tercieux, Camille and Vieilledent, Ghislain and Clark, Adam and Clark, James S. and Courbaud, Benoit and Fortunel, Claire and Kunstler, Georges and P\'elissier, Rapha\"el and R\"uger, Nadja and Mar\'echaux, Isabelle},
     title = {Beyond variance: simple random distributions are not a good proxy for intraspecific variability in systems with environmental structure},
     journal = {Peer Community Journal},
     eid = {e28},
     publisher = {Peer Community In},
     volume = {4},
     year = {2024},
     doi = {10.24072/pcjournal.360},
     language = {en},
     url = {https://peercommunityjournal.org/articles/10.24072/pcjournal.360/}
}
TY  - JOUR
AU  - Girard-Tercieux, Camille
AU  - Vieilledent, Ghislain
AU  - Clark, Adam
AU  - Clark, James S.
AU  - Courbaud, Benoit
AU  - Fortunel, Claire
AU  - Kunstler, Georges
AU  - Pélissier, Raphaël
AU  - Rüger, Nadja
AU  - Maréchaux, Isabelle
TI  - Beyond variance: simple random distributions are not a good proxy for intraspecific variability in systems with environmental structure
JO  - Peer Community Journal
PY  - 2024
VL  - 4
PB  - Peer Community In
UR  - https://peercommunityjournal.org/articles/10.24072/pcjournal.360/
DO  - 10.24072/pcjournal.360
LA  - en
ID  - 10_24072_pcjournal_360
ER  - 
%0 Journal Article
%A Girard-Tercieux, Camille
%A Vieilledent, Ghislain
%A Clark, Adam
%A Clark, James S.
%A Courbaud, Benoit
%A Fortunel, Claire
%A Kunstler, Georges
%A Pélissier, Raphaël
%A Rüger, Nadja
%A Maréchaux, Isabelle
%T Beyond variance: simple random distributions are not a good proxy for intraspecific variability in systems with environmental structure
%J Peer Community Journal
%D 2024
%V 4
%I Peer Community In
%U https://peercommunityjournal.org/articles/10.24072/pcjournal.360/
%R 10.24072/pcjournal.360
%G en
%F 10_24072_pcjournal_360
Girard-Tercieux, Camille; Vieilledent, Ghislain; Clark, Adam; Clark, James S.; Courbaud, Benoit; Fortunel, Claire; Kunstler, Georges; Pélissier, Raphaël; Rüger, Nadja; Maréchaux, Isabelle. Beyond variance: simple random distributions are not a good proxy for intraspecific variability in systems with environmental structure. Peer Community Journal, Volume 4 (2024), article  no. e28. doi : 10.24072/pcjournal.360. https://peercommunityjournal.org/articles/10.24072/pcjournal.360/

Peer reviewed and recommended by PCI : 10.24072/pci.ecology.100466

Conflict of interest of the recommender and peer reviewers:
The recommender in charge of the evaluation of the article and the reviewers declared that they have no conflict of interest (as defined in the code of conduct of PCI) with the authors or with the content of the article.

[1] Albert, C. H.; Grassein, F.; Schurr, F. M.; Vieilledent, G.; Violle, C. When and how should intraspecific variability be considered in trait-based plant ecology?, Perspectives in Plant Ecology, Evolution and Systematics, Volume 13 (2011) no. 3, pp. 217-225 | DOI

[2] Averill, C.; Fortunel, C.; Maynard, D. S.; van den Hoogen, J.; Dietze, M. C.; Bhatnagar, J. M.; Crowther, T. W. Alternative stable states of the forest mycobiome are maintained through positive feedbacks, Nature Ecology & Evolution, Volume 6 (2022) no. 4, pp. 375-382 | DOI

[3] Banitz, T. Spatially structured intraspecific trait variation can foster biodiversity in disturbed, heterogeneous environments, Oikos, Volume 128 (2019) no. 10, pp. 1478-1491 | DOI

[4] Barbier, M. Two paradigms for intraspecific variability., Peer Community in Ecology (2024) | DOI

[5] Bartlett, M. K.; Zhang, Y.; Yang, J.; Kreidler, N.; Sun, S.; Lin, L.; Hu, Y.; Cao, K.; Sack, L. Drought tolerance as a driver of tropical forest assembly: resolving spatial signatures for multiple processes, Ecology, Volume 97 (2016) no. 2, pp. 503-514 | DOI

[6] Bolnick, D. I.; Amarasekare, P.; Araújo, M. S.; Bürger, R.; Levine, J. M.; Novak, M.; Rudolf, V. H.; Schreiber, S. J.; Urban, M. C.; Vasseur, D. A. Why intraspecific trait variation matters in community ecology, Trends in Ecology & Evolution, Volume 26 (2011) no. 4, pp. 183-192 | DOI

[7] Bonnier, G. Cultures expérimentales dans les Alpes et les Pyrénées, Revue générale de Botanique, Volume Tome 2 (1890), pp. 513-546

[8] Chesson, P. Mechanisms of Maintenance of Species Diversity, Annual Review of Ecology and Systematics, Volume 31 (2000) no. 1, pp. 343-366 | DOI

[9] Clark, J. S. Individuals and the variation needed for high species diversity in forest trees, Science, Volume 327 (2010) no. 5969, pp. 1129-1132 | DOI

[10] Clark, J. S.; Dietze, M.; Chakraborty, S.; Agarwal, P. K.; Ibanez, I.; LaDeau, S.; Wolosin, M. Resolving the biodiversity paradox, Ecology Letters, Volume 10 (2007) no. 8, pp. 647-659 | DOI

[11] Clark, J. S.; Mohan, J.; Dietze, M.; Ibanez, I. Coexistence : How to indentify trophic trade-offs., Ecology, Volume 84 (2003) no. 1, pp. 17-31 | DOI

[12] Courbaud, B.; Vieilledent, G.; Kunstler, G. Intra-specific variability and the comp­e­ti­tion–co­lo­ni­sa­tion trade-off: coexistence, abundance and stability patterns, Theoretical Ecology, Volume 5 (2012) no. 1, pp. 61-71 | DOI

[13] Craine, J. M. Resource Strategies of Wild Plants:, Princeton University Press, Princeton, 2009

[14] Crawford, M. S.; Jeltsch, F.; May, F.; Grimm, V.; Schlägel, U. E. Intraspecific trait variation increases species diversity in a trait-based grassland model, Oikos, Volume 128 (2019) no. 3, pp. 441-455 | DOI

[15] De Frenne, P.; Lenoir, J.; Luoto, M.; Scheffers, B. R.; Zellweger, F.; Aalto, J.; Ashcroft, M. B.; Christiansen, D. M.; Decocq, G.; De Pauw, K.; Govaert, S.; Greiser, C.; Gril, E.; Hampe, A.; Jucker, T.; Klinges, D. H.; Koelemeijer, I. A.; Lembrechts, J. J.; Marrec, R.; Meeussen, C.; Ogée, J.; Tyystjärvi, V.; Vangansbeke, P.; Hylander, K. Forest microclimates and climate change: Importance, drivers and future research agenda, Global Change Biology, Volume 27 (2021) no. 11, pp. 2279-2297 | DOI

[16] Des Roches, S.; Post, D. M.; Turley, N. E.; Bailey, J. K.; Hendry, A. P.; Kinnison, M. T.; Schweitzer, J. A.; Palkovacs, E. P. The ecological importance of intraspecific variation, Nature Ecology & Evolution, Volume 2 (2018) no. 1, pp. 57-64 | DOI

[17] Detto, M.; Levine, J. M.; Pacala, S. W. Maintenance of high diversity in mechanistic forest dynamics models of competition for light, Ecological Monographs, Volume 92 (2022) no. 2, p. e1500 | DOI

[18] Ehlers, B. K.; Damgaard, C. F.; Laroche, F. Intraspecific genetic variation and species coexistence in plant communities, Biology Letters, Volume 12 (2016) no. 1, p. 20150853 | DOI

[19] Estes, L.; Elsen, P. R.; Treuer, T.; Ahmed, L.; Caylor, K.; Chang, J.; Choi, J. J.; Ellis, E. C. The spatial and temporal domains of modern ecology, Nature Ecology & Evolution, Volume 2 (2018) no. 5, pp. 819-826 | DOI

[20] Falster, D. S.; Brännström, A.; Westoby, M.; Dieckmann, U. Multitrait successional forest dynamics enable diverse competitive coexistence, Proceedings of the National Academy of Sciences, Volume 114 (2017) no. 13, p. E2719-E2728 | DOI

[21] Fortunel, C.; Lasky, J. R.; Uriarte, M.; Valencia, R.; Wright, S. J.; Garwood, N. C.; Kraft, N. J. B. Topography and neighborhood crowding can interact to shape species growth and distribution in a diverse Amazonian forest, Ecology, Volume 99 (2018) no. 10, pp. 2272-2283 | DOI

[22] Girard-Tercieux, C.; Vieilledent, G. Scripts and codes used for "Beyond variance: simple random distributions are not a good proxy for intraspecific variability in systems with environmental structure", Zenodo, 2023 | DOI

[23] Girard-Tercieux, C.; Vieilledent, G.; Clark, A. T.; Clark, J. S.; Courbaud, B.; Fortunel, C.; Kunstler, G.; Pélissier, R.; Rüger, N.; Maréchaux, I. Supplementary information for "Beyond variance: simple random distributions are not a good proxy for intraspecific variability in systems with environmental structure", bioRxiv, 2024 (https://www.biorxiv.org/content/10.1101/2022.08.06.503032v5.supplementary-material)

[24] Girard‐Tercieux, C.; Maréchaux, I.; Clark, A. T.; Clark, J. S.; Courbaud, B.; Fortunel, C.; Guillemot, J.; Künstler, G.; le Maire, G.; Pélissier, R.; Rüger, N.; Vieilledent, G. Rethinking the nature of intraspecific variability and its consequences on species coexistence, Ecology and Evolution, Volume 13 (2023) no. 3, p. e9860 | DOI

[25] Hart, S.; Schreiber, S.; Levine, J. How variation between individuals affects species coexistence, Ecology letters, Volume 19 (2016) no. 8, pp. 825-838 | DOI

[26] Hubbell, S. P. The Unified Neutral Theory of Biodiversity and Biogeography (MPB-32), Princeton University Press, 2001

[27] Hurtt, G. C.; Pacala, S. W. The consequences of recruitment limitation: reconciling chance, history and competitive differences between plants, Journal of Theoretical Biology, Volume 176 (1995) no. 1, pp. 1-12 | DOI

[28] Jung, V.; Violle, C.; Mondy, C.; Hoffmann, L.; Muller, S. Intraspecific variability and trait-based community assembly, Journal of Ecology, Volume 98 (2010) no. 5, pp. 1134-1140 | DOI

[29] Kropotkine, P. De Darwin à Lamarck: Kropotkine biologiste (1910-1919), ENS Éditions, 2015 | DOI

[30] Lichstein, J.; Dushoff, J.; Levin, S.; Pacala, S. Intraspecific variation and species coexistence, American Naturalist, Volume 170 (2007) no. 6, pp. 807-818 | DOI

[31] Marrot, P.; Latutrie, M.; Piquet, J.; Pujol, B. Natural selection fluctuates at an extremely fine spatial scale inside a wild population of snapdragon plants, Evolution, Volume 76 (2021) no. 3, pp. 658-666 | DOI

[32] Moran, E. V.; Hartig, F.; Bell, D. M. Intraspecific trait variation across scales: implications for understanding global change responses, Global Change Biology, Volume 22 (2016) no. 1, pp. 137-150 | DOI

[33] Napier, J. D.; Heckman, R. W.; Juenger, T. E. Gene-by-environment interactions in plants: Molecular mechanisms, environmental drivers, and adaptive plasticity, The Plant Cell, Volume 35 (2023) no. 1, pp. 109-124 | DOI

[34] Nicotra, A. B.; Atkin, O. K.; Bonser, S. P.; Davidson, A. M.; Finnegan, E. J.; Mathesius, U.; Poot, P.; Purugganan, M. D.; Richards, C. L.; Valladares, F.; van Kleunen, M. Plant phenotypic plasticity in a changing climate, Trends in Plant Science, Volume 15 (2010) no. 12, pp. 684-692 | DOI

[35] Niinemets, Ü. Is there a species spectrum within the world‐wide leaf economics spectrum? Major variations in leaf functional traits in the Mediterranean sclerophyll Quercus ilex, New Phytologist, Volume 205 (2015) no. 1, pp. 79-96 | DOI

[36] Poorter, L.; Castilho, C. V.; Schietti, J.; Oliveira, R. S.; Costa, F. R. C. Can traits predict individual growth performance? A test in a hyperdiverse tropical forest, New Phytologist, Volume 219 (2018) no. 1, pp. 109-121 | DOI

[37] Purves, D. W.; Vanderwel, M. C. Traits States and Rates: Understanding Coexistence in Forests, In Forests and Global Change. Cambridge University Press, British Ecological Society Edition (2014) | DOI

[38] Raffard, A.; Santoul, F.; Cucherousset, J.; Blanchet, S. The community and ecosystem consequences of intraspecific diversity: a meta-analysis: The ecological effects of intraspecific diversity, Biological Reviews, Volume 94 (2019) no. 2, pp. 648-661 | DOI

[39] Rixen, C.; Wipf, S.; Rumpf, S. B.; Giejsztowt, J.; Millen, J.; Morgan, J. W.; Nicotra, A. B.; Venn, S.; Zong, S.; Dickinson, K. J. M.; Freschet, G. T.; Kurzböck, C.; Li, J.; Pan, H.; Pfund, B.; Quaglia, E.; Su, X.; Wang, W.; Wang, X.; Yin, H.; Deslippe, J. R. Intraspecific trait variation in alpine plants relates to their elevational distribution, Journal of Ecology, Volume 110 (2022) no. 4, pp. 860-875 | DOI

[40] Roswell, M.; Dushoff, J.; Winfree, R. A conceptual guide to measuring species diversity, Oikos, Volume 130 (2021) no. 3, pp. 321-338 | DOI

[41] Rüger, N.; Condit, R.; Dent, D. H.; DeWalt, S. J.; Hubbell, S. P.; Lichstein, J. W.; Lopez, O. R.; Wirth, C.; Farrior, C. E. Demographic trade-offs predict tropical forest dynamics, Science, Volume 368 (2020) no. 6487, pp. 165-168 | DOI

[42] Rüger, N.; Huth, A.; Hubbell, S. P.; Condit, R. Response of recruitment to light availability across a tropical lowland rain forest community, Journal of Ecology, Volume 97 (2009) no. 6, pp. 1360-1368 | DOI

[43] Schmitt, S.; Tysklind, N.; Hérault, B.; Heuertz, M. Topography drives microgeographic adaptations of closely related species in two tropical tree species complexes, Molecular Ecology, Volume 30 (2021) no. 20, pp. 5080-5093 | DOI

[44] Siefert, A.; Violle, C.; Chalmandrier, L.; Albert, C. H.; Taudiere, A.; Fajardo, A.; Aarssen, L. W.; Baraloto, C.; Carlucci, M. B.; Cianciaruso, M. V.; Dantas, V. d. L.; Bello, F. d.; Duarte, L. D. S.; Fonseca, C. R.; Freschet, G. T.; Gaucherand, S.; Gross, N.; Hikosaka, K.; Jackson, B.; Jung, V.; Kamiyama, C.; Katabuchi, M.; Kembel, S. W.; Kichenin, E.; Kraft, N. J. B.; Lagerström, A.; Bagousse‐Pinguet, Y. L.; Li, Y.; Mason, N.; Messier, J.; Nakashizuka, T.; Overton, J. M.; Peltzer, D. A.; Pérez‐Ramos, I. M.; Pillar, V. D.; Prentice, H. C.; Richardson, S.; Sasaki, T.; Schamp, B. S.; Schöb, C.; Shipley, B.; Sundqvist, M.; Sykes, M. T.; Vandewalle, M.; Wardle, D. A. A global meta-analysis of the relative extent of intraspecific trait variation in plant communities, Ecology Letters, Volume 18 (2015) no. 12, pp. 1406-1419 | DOI

[45] Soong, J. L.; Janssens, I. A.; Grau, O.; Margalef, O.; Stahl, C.; Van Langenhove, L.; Urbina, I.; Chave, J.; Dourdain, A.; Ferry, B.; Freycon, V.; Herault, B.; Sardans, J.; Peñuelas, J.; Verbruggen, E. Soil properties explain tree growth and mortality, but not biomass, across phosphorus-depleted tropical forests, Scientific Reports, Volume 10 (2020), p. 2302 | DOI

[46] Stump, S. M.; Song, C.; Saavedra, S.; Levine, J. M.; Vasseur, D. A. Synthesizing the effects of individual‐level variation on coexistence, Ecological Monographs, Volume 92 (2022) no. 1 | DOI

[47] Tymen, B.; Vincent, G.; Courtois, E. A.; Heurtebize, J.; Dauzat, J.; Marechaux, I.; Chave, J. Quantifying micro-environmental variation in tropical rainforest understory at landscape scale by combining airborne LiDAR scanning and a sensor network, Annals of Forest Science, Volume 74 (2017) no. 2, p. 32 | DOI

[48] Uriarte, M.; Menge, D. Variation between individuals fosters regional species coexistence, Ecology Letters, Volume 21 (2018) no. 10, pp. 1496-1504 | DOI

[49] Vieilledent, G.; Courbaud, B.; Kunstler, G.; Dhôte, J.-F.; Clark, J. S. Individual variability in tree allometry determines light resource allocation in forest ecosystems: a hierarchical Bayesian approach, Oecologia, Volume 163 (2010) no. 3, pp. 759-773 | DOI

[50] Violle, C.; Enquist, B.; McGill, B.; Jiang, L.; Albert, C.; Hulshof, C.; Jung, V.; Messier, J. The return of the variance: Intraspecific variability in community ecology, Trends in Ecology and Evolution, Volume 27 (2012) no. 4, pp. 244-252 | DOI

[51] Westerband, A. C.; Funk, J. L.; Barton, K. E. Intraspecific trait variation in plants: a renewed focus on its role in ecological processes, Annals of Botany, Volume 127 (2021) no. 4, pp. 397-410 | DOI

[52] Wiegand, T.; Wang, X.; Anderson-Teixeira, K. J.; Bourg, N. A.; Cao, M.; Ci, X.; Davies, S. J.; Hao, Z.; Howe, R. W.; Kress, W. J.; Lian, J.; Li, J.; Lin, L.; Lin, Y.; Ma, K.; McShea, W.; Mi, X.; Su, S.-H.; Sun, I.-F.; Wolf, A.; Ye, W.; Huth, A. Consequences of spatial patterns for coexistence in species-rich plant communities, Nature Ecology & Evolution, Volume 5 (2021), pp. 965-973 | DOI

[53] Zellweger, F.; De Frenne, P.; Lenoir, J.; Rocchini, D.; Coomes, D. Advances in Microclimate Ecology Arising from Remote Sensing, Trends in Ecology & Evolution, Volume 34 (2019) no. 4, pp. 327-341 | DOI

Cited by Sources: