Skip to main content
Log in

Plasticity in apical dominance and damage tolerance under variable resource availability in Medicago truncatula

  • Published:
Plant Ecology Aims and scope Submit manuscript

Abstract

The activation of dormant meristems following apical damage is an important mechanism for tolerance of herbivore damage, but its impact could vary with resource availability. Here, we examined central predictions of the limiting resource model (LRM), according to which high resource availability can support damage tolerance in plants with deterministic apical dominance, but will have limited or no effect in plants that are induced to increase branching by increased resource availability regardless of damage. We examined these predictions by studying the branching patterns of Medicago truncatula plants in response to both light and water availabilities and their effects on tolerance of apical damage. We used plants from environments that were predicted to select for different levels of apical dominance. Intact plants from the more productive and competitive population exhibited strong apical dominance and refrained from branching even under full light, whereas plants from the less productive and sparser population exhibited greater plasticity in apical dominance and readily branched under high water and light. In accordance with the LRM, these differences translated into differential responsiveness to apical damage: given abundant water, apical damage induced the activation of lateral meristems and increased pod and seed production in plants from the more productive environment, but not in plants from the less productive environment. These results suggest an adaptive association between deterministic inhibition of lateral meristems and compensatory ability, which supports the hypothesis that greater compensatory responsiveness to apical damage could be a derivative of adaptation to other environmental stresses, such as light competition.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Aarssen LW (1995) Hypotheses for the evolution of apical dominance in plants: implications for the interpretation of overcompensation. Oikos 74:149–156

    Article  Google Scholar 

  • Aarssen LW, Irwin DL (1991) What selection: herbivory or competition. Oikos 60:261–262

    Article  Google Scholar 

  • Alpert P, Simms EL (2002) The relative advantages of plasticity and fixity in different environments: when is it good for a plant to adjust? Evol Ecol 16:285–297

    Article  Google Scholar 

  • Amir S, Cohen D (1990) Optimal reproductive efforts and the timing of reproduction of annual plants in randomly varying environments. J Theor Biol 147:17–42

    Article  Google Scholar 

  • Aronson JA, Kigel J, Shmida A (1990) Comparative plant sizes and reproductive strategies in desert and Mediterranean populations of ephemeral plants. Isr J Bot 39:413–430

    Google Scholar 

  • Banta JA, Stevens MHH, Pigliucci M (2010) A comprehensive test of the ‘limiting resources’ framework applied to plant tolerance to apical meristem damage. Oikos 119:359–369

    Article  Google Scholar 

  • Belsky AJ (1986) Does herbivory benefit plants: a review of the evidence. Am Nat 127:870–892

    Article  Google Scholar 

  • Bigger DS, Marvier MA (1998) How different would a world without herbivory be? A search for generality in ecology. Integr Biol 1:60–67

    Article  Google Scholar 

  • Bradshaw AD (1965) Evolutionary significance of phenotypic plasticity in plants. Advan Genet 13:115–155

    Article  Google Scholar 

  • Bruins HJ (1990) The impact of man and climate on the central Negev and northeastern Sinai Deserts during the late Holocene. In: Bottenma SS, Entjes-Nielborg G, van Zeist W (eds) Man’s role in the shaping of the Eastern Mediterranean landscape. Balkema, Rotterdam, pp 87–99

    Google Scholar 

  • Cohen D (1971) Maximizing final yield when growth is limited by time or by limiting resources. J Theor Biol 33:299–307

    Article  PubMed  CAS  Google Scholar 

  • Crawley MJ (1983) Herbivory: The dynamics of animal–plant interactions. Blackwell, Oxford

    Google Scholar 

  • Ferraro DO, Oesterheld M (2002) Effect of defoliation on grass growth. A quantitative review. Oikos 98:125–133

    Article  Google Scholar 

  • Gambash S, Kochba M, Avnimelech Y (1990) Studies on slow-release fertilizers: II. A method for evaluation of nutrient release rate from slow-releasing fertilizers. Soil Sci 150:446–450

    Article  CAS  Google Scholar 

  • Goldshleger N, Ben-Dor E, Benyamini Y, Agassi M (2004) Soil reflectance as a tool for assessing physical crust arrangement of four typical soils in Israel. Soil Sci 169:677–687

    Article  CAS  Google Scholar 

  • Grime JP (1979) Plant strategies and vegetation processes. John Wiley & Sons, Chichester

    Google Scholar 

  • Hawkes CV, Sullivan JJ (2001) The impact of herbivory on plants in different resource conditions: a meta-analysis. Ecology 82:2045–2058

    Article  Google Scholar 

  • Hilbert DW, Swift DM, Detling JK, Dyer MI (1981) Relative growth-rates and the grazing optimization hypothesis. Oecologia 51:14–18

    Article  Google Scholar 

  • Huhta AP, Lennartsson T, Tuomi J, Rautio P, Laine K (2000) Tolerance of Gentianella campestris in relation to damage intensity: an interplay between apical dominance and herbivory. Evol Ecol 14:373–392

    Article  Google Scholar 

  • Johnson EA, Miyanishi K (2007) Plant disturbance ecology: the process and the response. Elsevier, Burlington

    Google Scholar 

  • Juenger T, Bergelson J (2000) The evolution of compensation to herbivory in scarlet gilia, Ipomopsis aggregata: herbivore-imposed natural selection and the quantitative genetics of tolerance. Evolution 54:764–777

    PubMed  CAS  Google Scholar 

  • Karban R, Baldwin IT (1997) Induced responses to herbivory. University of Chicago Press, Chicago

    Google Scholar 

  • King D, Roughgarden J (1982) Graded allocation between vegetative and reproductive growth for annual plants in growing seasons of random length. Theor Popul Biol 22:1–16

    Article  Google Scholar 

  • Kirk RE (1995) Experimental design: procedures for the behavioral sciences. Brooks/Cole, Pacific Grove, CA

    Google Scholar 

  • Lesins KA, Lesins I (1979) Genus medicago leguminosae. Dr. W. Junk, The Hague

    Google Scholar 

  • Limami AM, Ricoult C, Planchet E, et al (2007) Response of Medicago truncatula to abiotic stress. The Medicago truncatula handbook. http://www.noble.org/MedicagoHandbook/. Accessed 11 April 2010

  • Maschinski J, Whitham TG (1989) The continuum of plant-responses to herbivory: the influence of plant-association, nutrient availability, and timing. Am Nat 134:1–19

    Article  Google Scholar 

  • McConnaughay KDM, Coleman JS (1999) Biomass allocation in plants: ontogeny or optimality? A test along three resource gradients. Ecology 80:2581–2593

    Article  Google Scholar 

  • Moreau D (2006) Morphology, development and plant architecture of M. truncatula. The Medicago truncatula handbook. http://www.noble.org/MedicagoHandbook/. Accessed 1 Mar 2010

  • Novoplansky A (1996) Developmental responses of individual Onobrychis plants to spatial heterogeneity. Vegetatio 127:31–39

    Article  Google Scholar 

  • Novoplansky A (2002) Developmental plasticity in plants: implications of non-cognitive behavior. Evol Ecol 3:177–188

    Article  Google Scholar 

  • Novoplansky A (2009) Picking battles wisely: plant behaviour under competition. Plant Cell Environ 32:726–741

    Article  PubMed  Google Scholar 

  • Novoplansky A, Cohen D, Sachs T (1994) Responses of an annual plant to temporal changes in light environment: an interplay between plasticity and determination. Oikos 69:437–446

    Article  Google Scholar 

  • Núñez-Farfán J, Fornoni J, Valverde PL (2007) The evolution of resistance and tolerance to herbivores. Annu Rev Ecol Evol Syst 38:541–566

    Article  Google Scholar 

  • Perevolotsky A, Seligman NG (1998) Role of grazing in Mediterranean rangeland ecosystems: inversion of a paradigm. Bioscience 48:1007–1017

    Article  Google Scholar 

  • Petrů M, Tielbörger K, Belkin R, Sternberg M, Jeltsch F (2006) Life history variation in an annual plant under two opposing environmental constraints along an aridity gradient. Ecography 29:66–74

    Article  Google Scholar 

  • Pigliucci M (1998) Developmental phenotypic plasticity: where internal programming meets the external environment. Curr Opin Plant Biol 1:87–91

    Article  PubMed  CAS  Google Scholar 

  • Polley HW, Detling JK (1988) Herbivory tolerance of Agropyron smithii populations with different grazing histories. Oecologia 77:261–267

    Article  Google Scholar 

  • Rautio P, Huhta AP, Piippo S et al (2005) Overcompensation and adaptive plasticity of apical dominance in Erysimum strictum (Brassicaceae) in response to simulated browsing and resource availability. Oikos 111:179–191

    Article  Google Scholar 

  • Rolston MP (1978) Water impermeable seed dormancy. Bot Rev 44:365–396

    Article  CAS  Google Scholar 

  • Scheiner SM (2001) MANOVA: multiple response variables and multispecies interactions. In: Scheine SM, Gurevitch J (eds) Design and analysis of ecological experiments. Chapman & Hall, New York, pp 99–115

    Google Scholar 

  • Schmitt J (1997) Is photomorphogenic shade avoidance adaptive? Perspectives from population biology. Plant Cell Environ 20:826–830

    Article  Google Scholar 

  • Stowe KA, Marquis RJ, Hochwender CG, Simms EL (2000) The evolutionary ecology of tolerance to consumer damage. Ann Rev Ecol Syst 31:565–595

    Article  Google Scholar 

  • Strauss SY, Agrawal AA (1999) The ecology and evolution of plant tolerance to herbivory. Trends Ecol Evol 14:179–185

    Article  PubMed  Google Scholar 

  • Sultan SE (2010) Plant developmental responses to the environment: eco-devo insights. Curr Opin Plant Biol 13:96–101

    Article  PubMed  CAS  Google Scholar 

  • Tiffin P (2000) Mechanisms of tolerance to herbivore damage: what do we know? Evol Ecol 14:523–536

    Article  Google Scholar 

  • Trumble JT, Kolodnyhirsch DM, Ting IP (1993) Plant compensation for arthropod herbivory. Annu Rev Entomo 38:93–119

    Article  Google Scholar 

  • Weijschede J, Martinkova J, de Kroon H, Huber H (2008) Effects of cell number and cell size on petiole length variation in a stoloniferous herb. Am J Bot 95:41–49

    Article  PubMed  Google Scholar 

  • Wienig C (2000) Plasticity versus canalization: population differences in the timing of shade-avoidance responses. Evolution 54:441–451

    Google Scholar 

  • Wise MJ, Abrahamson WG (2005) Beyond the compensatory continuum: environmental resource levels and plant tolerance of herbivory. Oikos 109:417–428

    Article  Google Scholar 

  • Wise MJ, Abrahamson WG (2007) Effects of resource availability on tolerance of herbivory: a review and assessment of three opposing models. Am Nat 169:443–454

    Article  PubMed  Google Scholar 

  • Wise MJ, Abrahamson WG (2008) Applying the limiting resource model to plant tolerance of apical meristem damage. Am Nat 172:635–647

    Article  PubMed  Google Scholar 

  • Zar JH (1999) Biostatistical analysis. Prentice Hall, Upper Saddle River, NJ

    Google Scholar 

  • Zohary M (1987) Flora Palaestina, vol 2. Jerusalem, Israel Academy of Sciences and Humanities

    Google Scholar 

Download references

Acknowledgments

We thank Omer Falik, Hagai Shemesh and Itamar Giladi for the stimulating discussions, Eliah Malka and Tali Brunner for helpful comments on early versions of the manuscript and Tania Acuña and Efrat Elimelech for the dedicated technical help. The study was supported in part by a research grant from the Israel Science Foundation to A.N. This is publication no. 732 of the Mitrani Department of Desert Ecology.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Michal Gruntman.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PPT 128 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Gruntman, M., Shirata, C. & Novoplansky, A. Plasticity in apical dominance and damage tolerance under variable resource availability in Medicago truncatula . Plant Ecol 212, 1537–1548 (2011). https://doi.org/10.1007/s11258-011-9929-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11258-011-9929-8

Keywords

Navigation