Abstract
How plants respond to density via modular plasticity is obscure, probably because relevant studies using covariance analysis (ANCOVA) and allometric analysis rarely focus on multiple stages of plant growth, and also the two approaches are seldom used simultaneously. In this study, a field experiment evaluated the effects of three density levels on resource allocation traits in Abutilon theophrasti and tested the degree to which these were explained by indirect effects of density on biomass over time. Results showed inconsistent responses in allocation traits and allometric relationships at each growth stage. At 30 days of plant growth, high density increased root/stem, root/leaf, and stem/leaf, but did not affect any allometric relationships. At 50 days, density altered most mass and ratio traits, but not for allometric exponents. At 70 days, density altered allometric relationships, but did not affect plant allocation patterns. The stage-dependent allometric relationships and the fact that allocation plasticity and allometric plasticity did not coincide both suggested that one-stage allometric plasticity might be apparent plasticity. In response to the increase of density, plants first altered the strategy of biomass partitioning and then growth rate or developmental stage, indicating that density effects intensified over time. For plasticity in a modular trait, size effects can be regarded as a component of (indirect) environmental effects, with the residual variation after removal of size effects being the other component of plant (direct) active response. The insights into apparent plasticity of allometry and two components of plasticity should be of essential importance to investigating phenotypic plasticity and its ecological and evolutionary implications.
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References
Aerts R (1999) Interspecific competition in natural plant communities: mechanisms, trade-offs and plant-soil feedbacks. J Exp Bot 50:29–37
Álvarez-Cansino L, Zunzunegui M, Barradas MCD, Esquivias MP (2010) Gender-specific costs of reproduction on vegetative growth and physiological performance in the dioecious shrub Corema album. Ann Bot 106:989–998
Arenas F, Viejo RM, Fernández C (2002) Density-dependent regulation in an invasive seaweed: responses at plant and modular levels. J Ecol 90:820–829
Auffray JC, Debat V, Alibert P (1999) Shape asymmetry and developmental stability. In: Chaplain MAJ (ed) On growth and form: spatiotemporal patterning in biology. Wiley, Chichester, pp 309–324
Bell DL, Galloway LF (2007) Plasticity to neighbour shade: fitness consequences and allometry. Funct Ecol 21:1146–1153
Berendse F, Möller F (2009) Effects of competition on root-shoot allocation in Plantago lanceolata L.: adaptive plasticity or ontogenetic drift? Plant Ecol 201:567–573
Bloom AJ, Chapin FS, Mooney HA (1985) Resource limitations in plants—an economic analogy. Annu Rev Ecol Syst 16:363–392
Bouvet J-M, Vigneron P, Saya A (2005) Phenotypic plasticity of growth trajectory and ontogenic allometry in response to density for eucalyptus hybrid clones and families. Ann Bot 96:811–821
Bradshaw AD (1965) Evolutionary significance of phenotypic plasticity in plants. Adv Gen 13:155
Cahill JF Jr (2003) Lack of relationship between below-ground competition and allocation to roots in 10 grassland species. J Ecol 91:532–540
Casper BB, Jackson RB (1997) Plant competition underground. Annu Rev Ecol Syst 28:545–570
Casper BB, Cahill JF Jr, Hyatt LA (1998) Above-ground competition does not alter biomass allocated to roots in Abutilon theophrasti. New Phytol 140:231–238
Cheplick GP (2006) A modular approach to biomass allocation in an invasive annual (Microstegium vimineum; Poaceae). Am J Bot 93:539–545
Cheplick GP (2020) Life-history variation in a native perennial grass (Tridens flavus): reproductive allocation, biomass partitioning, and allometry. Plant Ecol 221:103–115
Coleman JS, McConnaughay KDM, Ackerly DD (1994) Interpreting phenotypic variation in plants. Trends Ecol Evol 9:187–191
Conover DO, Schultz ET (1995) Phenotypic similarity and the evolutionary significance of countergradient variation. Trends Ecol Evol 10(6):248–252
de Kroon, H, Huber H, Stuefer JF Van Groenendael JM (2005) A modular concept of phenotypic plasticity in plants. New Phytol 166(1):73–82
Debat V, David P (2001) Mapping phenotypes: canalization, plasticity and developmental stability. Trends Ecol Evol 16(10):555–561
Donald CM (1958) The interaction of competition for light and for nutrients. Aust J Agric Res 9:421–435
Dybzinski R, Farrior C, Wolf A, Reich PB, Pacala SW (2011) Evolutionarily stable strategy of carbon allocation to foliage, wood, and fine roots in trees competing for light and nitrogen: an analytically tractable, individual-based model and quantitative comparisons to data. Am Nat 177:153–166
Elgart M, Snir O, Soen Y (2015) Stress-mediated tuning of developmental robustness and plasticity in flies. Biochim et Biophys Acta—Gene Regul Mech 1849:462–466
Enquist BJ, Niklas KJ (2001) Invariant scaling relations across tree-dominated communities. Nature 410:655–660
Forster MA, Ladd B, Bonser SP (2011) Optimal allocation of resources in response to shading and neighbours in the heteroblastic species, Acacia implexa. Ann Bot 107:219–228
Fox JF (1995) Shoot demographic responses to manipulation of reproductive effort by bud removal in a willow. Oikos 72:283–287
Gersani M, Brown JS, Brien EO, Maina GM, Abramsky Z (2001) Tragedy of the commons as a result of root competition. J Ecol 89:660–669
Ghalambor CK, McKay JK, Carroll SP, Reznick DN (2007) Adaptive versus non-adaptive phenotypic plasticity and the potential for contemporary adaptation in new environments. Func Ecol 21(3):394–407
Gleason HA, Cronquist A (1991) Manual of vascular plants of northeastern United States and adjacent Canada. New York Botanical Garden, New York
Harper JL (1977) Population biology of plants. Academic Press, New York
Hill TD, Roberts BJ (2017) Effects of seasonality and environmental gradients on Spartina alterniflora allometry and primary production. Ecol Evol 7:9676–9688
Houle D, Jones LT, Fortune R, Sztepanacz JL (2019) Why does allometry evolve so slowly? Integr Comp Biol 59:1429–1440
Huang Y-X, Zhao X-Y, Zhou D-W, Luo Y-Y, Mao W (2010) Allometry of Corispermum macrocarpu in response to soil nutrient, water, and population density. Botany 88:13–19
Hulshof CM, Stegen JC, Swenson NG, Enquist CA, Enquist BJ (2012) Interannual variability of growth and reproduction in Bursera simaruba: the role of allometry and resource variability. Ecology 93:180–190
Hutchings MJ, Budd CSJ (1981) Plant competition and its course through time. Bioscience 31:640–645
Japhet W, Zhou D, Zhang H, Zhang H, Yu T (2009) Evidence of phenotypic plasticity in the response of Fagopyrum esculentum to population density and sowing date. J Plant Biol 52:303–311
Karlsson P, Méndez M (eds) (2005) The resource economy of plant reproduction. Elsevier, London
Kitano H (2004) Biological robustness. Nat Rev Genet 5:826–837
Kost C, de Oliveira EG, Knoch TA, Wirth R (2005) Spatio-temporal permanence and plasticity of foraging trails in young and mature leaf-cutting ant colonies (Atta spp.). J Trop Ecol 21:677–688
Laughlin DC, Gremer JR, Adler PB, Mitchell RM, Moore MM (2020) The net effect of functional traits on fitness. Trends Ecol Evol 36:1037–1047
Levins R (1968) Evolution in changing environments. Princeton University Press, Princeton
Li L, Weiner J, Zhou D, Huang Y, Sheng L (2013) Initial density affects biomass–density and allometric relationships in self-thinning populations of Fagopyrum esculentum. J Ecol 101:475–483
Li PF, Ma BL, Yan W, Cheng ZG, Li FM, Xiong YC (2016) Plant architecture, plasticity, and adaptation strategies of two oat genotypes under different competition intensities. J Sci Food Agric 96:1431–1439
Lines ER, Zavala MA, Purves DW, Coomes DA (2012) Predictable changes in aboveground allometry of trees along gradients of temperature, aridity and competition. Glob Ecol Biogeogr 21:1017–1028
Maliakal SK, McDonnell K, Dudley SA, Schmitt J (1999) Effects of red to far-red ratio and plant density on biomass allocation and gas exchange in Impatiens capensis. Int J Plant Sci 160:723–733
Masel J, Siegal ML (2009) Robustness: mechanisms and consequences. Trends Genet 25:395–403
Matsuyama S, Sakimoto M (2008) Allocation to reproduction and relative reproductive costs in two species of dioecious Anacardiaceae with contrasting phenology. Ann Bot 101:1391–1400
McCarthy MC, Enquist BJ (2007) Consistency between an allometric approach and optimal partitioning theory in global patterns of plant biomass allocation. Funct Ecol 21:713–720
McConnaughay KDM, Bazzaz FA (1992) The occupation and fragmentation of space: consequences of neighbouring shoots. Funct Ecol 6:711–718
McConnaughay KDM, Coleman JS (1999) Biomass allocation in plants: ontogeny or optimality? A test along three resource gradients. Ecology 80:2581–2593
Mestek BL, Barkoulas M (2016) The developmental genetics of biological robustness. Ann Bot 117:699–707
Morris EC (1999) Density-dependent mortality induced by low nutrient status of the substrate. Ann Bot 84:95–107
Müller I, Schmid B, Weiner J (2000) The effect of nutrient availability on biomass allocation patterns in 27 species of herbaceous plants. Perspect Plant Ecol, Evol Syst 3:115–127
Murphy GP, Dudley SA (2007) Above- and below-ground competition cues elicit independent responses. J Ecol 95:261–272
Navas ML, Garnier E (2002) Plasticity of whole plant and leaf traits in Rubia peregrina in response to light, nutrient and water availability. Acta Oecologica 23:375–383
Nicklas KJ (1994) Plant allometry: the scaling of form and process. University of Chicago, Chicago
Nicotra AB, Atkin OK, Bonser SP, Davidson AM, Finnegan EJ, Mathesius U, Poot P, Purugganan MD, Richards CL, ValladaresKleunen FMv (2010) Plant phenotypic plasticity in a changing climate. Trends Plant Sci 15:684–692
O’Brien EE, Gersani M, Brown JS (2005) Root proliferation and seed yield in response to spatial heterogeneity of below-ground competition. New Phytol 168:401–412
Ogawa K (2003) Size dependence of lead area and the mass of component organs during a course of self-thinning in a hinoki (Chamaecyparis obtusa) seedling population. Ecol Res 18:611–618
Palmer AR, Strobeck C (1986) Fluctuating asymmetry: measurement, analysis, patterns. Ann Rev Ecol Syst 17(1):391–421
Palmer AR (1994) Fluctuating asymmetry analysis: a primer. In: Markow TA (ed) Developmental instability: its origins and evolutionary implications. Kluwer Academic Publishers, Kluwer, Dordrecht, Netherlands. pp 335–364
Pigliucci M (2005) Evolution of phenotypic plasticity: where are we going now? Trends Ecol Evol 20:481–486
Pino J, Sans FX, Masalles RM (2002) Size-dependent reproductive pattern and short-term reproductive cost in Rumex obtusifolius L. Acta Oecologia 23:321–328
Poorter H, Niklas KJ, Reich PB, Oleksyn J, Poot P, Mommer L (2012) Biomass allocation to leaves, stems and roots: meta-analyses of interspecific variation and environmental control. New Phytol 193:30–50
Prescott CE, Grayston SJ, Helmisaari HS, Kaštovská E, Körner C, Lambers H, Meier IC, Millard P, Ostonen I (2020) Surplus carbon drives allocation and plant-soil interactions. Trends Ecol Evol 35:1110–1118
Price CA, Enquist BJ, Savage VM (2007) A general model for allometric covariation in botanical form and function. Proc Natl Acad Sci 104:13204–13209
Rudgers JA, Hallmark A, Baker SR, Baur L, Hall KM, Litvak ME, Muldavin EH, Pockman WT, Whitney KD (2019) Sensitivity of dryland plant allometry to climate. Funct Ecol 33:2290–2303
Shipley B, Meziane D (2002) The balanced-growth hypothesis and the allometry of leaf and root biomass allocation. Funct Ecol 16:326–331
Sides CB, Enquist BJ, Ebersole JJ, Smith MN, Henderson AN, Sloat LL (2014) Revisiting Darwin’s hypothesis: Does greater intraspecific variability increase species’ ecological breadth? Am J Bot 101:56–62
Smith DD (2020) Even when the seasons change our allometry stays the same. A Commentary on: “Corner’s rules pass the test of time: little effect of phenology on leaf-shoot and other scaling relationships.” Ann Bot 126:iii–iv
Thompson DB (2019) Diet-induced plasticity of linear static allometry is not so simple for grasshoppers: genotype-environment interaction in ontogeny is masked by convergent growth. Integr Comp Biol 59:1382–1398
Thornley JHM (1972) A balanced quantitative model for root: shoot ratios in vegetative plants. Ann Bot 36:431–441
Tilman D (1988) Plant strategies and the dynamics and structure of plant communities. Princeton University Press, Princeton
Tobler A, Nijhout HF (2010) Developmental constraints on the evolution of wing-body allometry in Manduca sexta. Evol Dev 12:592–600
Van Dongen S, Lens L (2000) The evolutionary potential of developmental instability. J Evol Biol 13:326–335
van Kleunen M, Fischer M (2005) Constraints on the evolution of adaptive phenotypic plasticity in plants. New Phytol 166:49–60
Vasseur F, Exposito-Alonso M, Ayala-Garay OJ, Wang G, Enquist BJ, Vile D, Violle C, Weigel D (2018) Adaptive diversification of growth allometry in the plant Arabidopsis thaliana. Proc Natl Acad Sci 115:3416–3421
Vea IM, Shingleton AW (2020) Network-regulated organ allometry: the developmental regulation of morphological scaling. Wiley Interdiscip Rev. https://doi.org/10.1002/wdev.391
Vizcaíno-Palomar N, Ibáñez I, González-Martínez SC, Zavala MA, Alía R (2016) Adaptation and plasticity in aboveground allometry variation of four pine species along environmental gradients. Ecol Evol 6:7561–7573
Voje KL, Hansen TF, Egset CK, Bolstad GH, Pelabon C (2013) Allometric constraints and the evolution of allometry. Evolution 68:866–885
Waddington CH (1942) Canalization of development and the inheritance of acquired characters. Nature 150(3811):563–565
Wang T-H (2006) The study of plant phenotypic plasticity and life-history strategies. Northeast Normal University, Changchun
Wang T-H, Zhou D-W, Wang P, Zhang H-X (2006) Size-dependent reproductive effort in Amaranthus retroflexus: the fluence of planting density and sowing date. Can J Bot 84:485–492
Wang S, Li L, Zhou D-W (2017) Morphological plasticity in response to population density varies with soil conditions and growth stage in Abutilon theophrasti (Malvaceae). Plant Ecol 218:785–797
Wang S, Li L, Zhou D-W (2021) Root morphological responses to population density vary with soil conditions and growth stages: the complexity of density effects. Ecol Evol. https://doi.org/10.22541/au.160010745.59435642
Wang S, Callaway RM (2021) Plasticity in response to plant-plant interactions and water availability. Ecology. https://doi.org/10.1002/ecy.3361
Weijschedé J, MartínkováKroon JHd, Huber H (2006) Shade avoidance in Trifolium repens: costs and benefits of plasticity in petiole length and leaf size. New Phytol 172:655–666
Weiner J (2004) Allocation, plasticity and allometry in plants. Perspect Plant Ecol Evol Syst 6:207–215
Weiner J, Fishman L (1994) Competition and allometry in Kochia scoporia. Ann Bot 73:263–271
Weiner J, Thomas SC (1992) Competition and allometry in three species of annual plants. Ecology 73:648–656
Weiner J, Campbell LG, Pino J, Echarte L (2009) The allometry of reproduction within plant populations. J Ecol 97:1220–1233
Wilkins AS (1997) Canalization: a molecular genetic perspective. BioEssays 19:257–262
Wright SD, McConnaughay KDM (2002) Interpreting phenotypic plasticity: the importance of ontogeny. Plant Species Biol 17:119–131
Yoda K, Kira T, Ogawa H, Hozumi K (1963) Self-thinning in overcrowded pure stands under cultivated and natural conditions. J Biol Osaka City Univ 14:107–129
Zhou D-W, Wang T-H, Valentine I (2005) Phenotypic plasticity of life-history characters in response to different germination timing in two annual weeds. Can J Bot 83:28–36
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We are grateful for the reviewers and editors who provided substantial elaborate and valuable comments on this manuscript.
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This work was funded by the National Natural Science Foundation of China (NSFC, 31800335), Guizhou Province Science and Technology Planning Program (2019-1089), Guizhou University Talent Introduction Research Program (2017-39), and Ecology Domestic First-class Discipline Construction Program (GNYL2017-007) to SW.
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Both authors contributed to the study conception and design. SW conducted the experiment, collected the data, and performed statistical analyses. The first draft of the manuscript was written and edited by SW. All authors read and approved the final manuscript.
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Wang, S., Zhou, DW. Stage-dependent plasticity in biomass allocation and allometry in response to population density in Abutilon theophrasti: a step forward to understanding the nature of phenotypic plasticity. Plant Ecol 222, 1157–1181 (2021). https://doi.org/10.1007/s11258-021-01168-8
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DOI: https://doi.org/10.1007/s11258-021-01168-8