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Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Development, photosynthetic activity and habitat selection of the clonal plant Fragaria vesca growing in copper-polluted soil

Sergio R. Roiloa A and Rubén Retuerto A B
+ Author Affiliations
- Author Affiliations

A Ecology Unit, Faculty of Biology, Santiago de Compostela University, 15782 Santiago de Compostela, Spain.

B Corresponding author. Email: bfretuer@usc.es

Functional Plant Biology 33(10) 961-971 https://doi.org/10.1071/FP06018
Submitted: 20 January 2006  Accepted: 7 June 2006   Published: 2 October 2006

Abstract

The ability of clonal systems to spread by ramet production may expose the clone to spatial heterogeneity. This study explored the physiological and morphological responses in the clonal plant Fragaria vesca L. growing in homogeneous (Cu-contaminated or uncontaminated) or in heterogeneous environments with patches of contrasting quality (Cu-contaminated or uncontaminated). We also investigated the potential of this species to selectively establish ramets within a heterogeneous environment. In heterogeneous environments, plants expanded ramets randomly, but selectively established ramets in the favourable patches. We discuss whether the selective establishment of ramets is a consequence of direct suppression of plant growth due to copper toxicity. The assimilate demand from offspring ramets in unfavourable environments increased the chlorophyll content and photosynthetic efficiency of parents by a feedback regulation process. Integration ameliorated the effects of copper on the photochemical efficiency of the offspring ramets. We did not observe integration costs, in terms of total biomass, for parents supporting ramets in Cu-contaminated environments, although we did detect costs in terms of ramet production. Parents with offspring ramets in Cu-contaminated environments produced 25 times more reproductive biomass than parents with offspring ramets in uncontaminated environments. We interpret this as a strategy for escaping from stressful environments. In this study, we extend the concept of physiological integration in clonal plants to include photochemical responses.

Keywords: chlorophyll fluorescence, clonal plasticity, physiological integration, sink–source hypothesis.


Acknowledgments

We thank Raimundo Bermudez for field assistance, Alfonso Puñal, Mercedes Noya, Sandra González, Cristina Gianzo and Montserrat Bravo for help with the chemical analyses. SR Roiloa was supported by a grant from the Department of Education and Universities (Autonomous Government of Galicia). Two anonymous reviewers provided useful comments on the manuscript.


References


Alpert P (1996) Nutrient sharing in natural clonal fragments of Fragaria chiloensis. Journal of Ecology 84, 395–406.
Crossref |
open url image1

Alpert P (1999) Effects of clonal integration on plant plasticity in Fragaria chiloensis. Plant Ecology 141, 99–106.
Crossref | GoogleScholarGoogle Scholar | open url image1

Andrews JR, Fryer MJ, Baker NR (1995) Characterization of chilling effects on photosynthetic performance of maize crops during early season growth using chlorophyll fluorescence. Journal of Experimental Botany 46, 1195–1203. open url image1

Babani F, Lichtenthaler HK (1996) Light-induced and age-dependent development of chloroplasts in etiolated barley leaves as visualized by determination of photosynthetic pigments, CO2 assimilation rates and different kinds of chlorophyll fluorescence ratios. Journal of Plant Physiology 148, 555–566. open url image1

Bolhàr-Nordenkampf HR , Öquist G (1993) Chlorophyll fluorescence: a tool in photosynthesis research. In ‘Photosynthesis and production in a changing environment’. (Eds DO Hall, JMO Scurlock, HR Bolhár-Nordenkampf, RC Leegood, SP Long) pp. 193–206. (Chapman and Hall: London)

Bolhàr-Nordenkampf HR, Long SP, Baker NR, Öquist G, Scheiber U, Lechner EG (1989) Chlorophyll fluorescence as a probe of the photosynthetic competence of leaves in the field: a review of current instrumentation. Functional Ecology 3, 497–514.
Crossref |
open url image1

Briantais J , Vernotte C , Krause G , Weis E (1986) Chlorophyll a fluorescence of higher plants: chloroplasts and leaves. In ‘Light emission by plant and bacteria’. (Eds JA Govindjee, DJ Fork) pp. 539–583. (Academic Press: San Diego)

Butler W, Kitajima M (1975) Fluorescence quenching in photosystem II of chloroplasts. Biochimica et Biophysica Acta 376, 116–125.
PubMed |
open url image1

Caldwell MM , Pearcy RW (1994) ‘Exploitation of environmental heterogeneity by plants. Ecophysiological processes above and below ground.’ (Academic Press: San Diego)

Curran PJ, Dungan JL, Gholz HL (1990) Exploring the relationship between reflectance red edge and chlorophyll content in slash pine. Tree Physiology 7, 33–48.
PubMed |
open url image1

Day KJ, John EA, Hutchings MJ (2003) The effects of spatially heterogeneous nutrient supply on yield, intensity of competition and root placement patterns in Briza media and Festuca ovina. Functional Ecology 17, 454–463.
Crossref | GoogleScholarGoogle Scholar | open url image1

Demmig-Adams B, Máguas C, Adams WW, Meyer A, Kilian E, Lange OL (1990) Effect of high light on the efficiency of photochemical energy conversion in a variety of lichen species with green and blue–green phycobionts. Planta 180, 400–409.
Crossref | GoogleScholarGoogle Scholar | open url image1

Edwards GE, Baker NR (1993) Can CO2 assimilation in maize leaves be predicted accurately from chlorophyll fluorescence analysis? Photosynthesis Research 37, 89–102.
Crossref | GoogleScholarGoogle Scholar | open url image1

Eriksson O (1986) Mobility and space capture in the stoloniferous plant Potentilla anserine. Oikos 46, 82–87. open url image1

Evans JP, Cain ML (1995) A spatial test of foraging behavior in a clonal plant. Ecology 76, 1147–1155.
Crossref | GoogleScholarGoogle Scholar | open url image1

Fernandes JC, Henriques FS (1991) Biochemical, physiological, and structural effects of excess copper in plants. Botanical Review 57, 246–273. open url image1

Genty BE, Briantais JM, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochimica et Biophysica Acta 990, 87–92. open url image1

Hartgerink AP, Bazzaz FA (1984) Seedling-scale environmental heterogeneity influences individual fitness and population structure. Ecology 65, 198–206.
Crossref | GoogleScholarGoogle Scholar | open url image1

Harper JL (1977) ‘The population biology of plants.’ (Academic Press: London)

Hartnett DC, Bazzaz FA (1983) Physiological integration among intraclonal ramets in Solidago canadensis. Ecology 64, 779–788.
Crossref | GoogleScholarGoogle Scholar | open url image1

Hartnett DC, Bazzaz FA (1985) The integration of neighbourhood effects by clonal genets of Solidago canadensis. Journal of Ecology 73, 415–428.
Crossref |
open url image1

Horton P, Ruban AV (1992) Regulation of photosystem II. Photosynthesis Research 34, 375–385.
Crossref | GoogleScholarGoogle Scholar | open url image1

Humphrey LD, Pyke DA (1998) Demographic and growth responses of a guerrilla and a phalanx perennial grass in competitive mixtures. Journal of Ecology 86, 854–865.
Crossref | GoogleScholarGoogle Scholar | open url image1

Hurlbert SH (1984) Pseudoreplication and the design of ecological field experiments. Ecological Monographs 54, 187–211.
Crossref | GoogleScholarGoogle Scholar | open url image1

Hutchings MJ, de Kroon H (1994) Foraging in plants: the role of morphological plasticity in resources acquisition. Advances in Ecological Research 25, 159–238. open url image1

Jónsdóttir IS, Callaghan TV (1989) Localized defoliation stress and the movement of 14C-photoassimilates between tillers of Carex bigelowii. Oikos 54, 211–219. open url image1

Kleijn D, Van Groenendael JM (1999) The exploitation of heterogeneity by a clonal plant in habitats with contrasting productivity levels. Journal of Ecology 87, 873–884.
Crossref | GoogleScholarGoogle Scholar | open url image1

Kliměs L , Kliměsova J , Hendriks R , van Groenendael J (1997) Clonal plant architecture: a comparative analysis of form and function. In ‘The ecology and evolution of clonal plants’. (Eds H de Kroon, J van Groenendael) pp. 1–29. (Backhuys Publishers: Leiden)

Koivunen S, Saikkonen K, Vuorisalo T, Mutikainen P (2004) Heavy metals modify costs of reproduction and clonal growth in the stoloniferous herb Potentilla anserina. Evolutionary Ecology 18, 541–561.
Crossref | GoogleScholarGoogle Scholar | open url image1

Lambers H , Chapin FS , Pons TL (1998) ‘Plant physiological ecology.’ (Springer: New York)

Larcher W (1995) ‘Physiological plant ecology.’ (Springer: Berlin)

Lechowicz MJ, Bell G (1991) The ecology and genetics of fitness in forest plants. II. Microspatial heterogeneity of the edaphic environment. Journal of Ecology 79, 687–696.
Crossref |
open url image1

Lidon FC, Henriques FS (1992) Effects of excess copper on the photosynthetic pigments in rice plants. Botanical Bulletin 33, 141–149. open url image1

Maksymiec W (1997) Effect of copper on cellular processes in higher plants. Photosynthetica 34, 321–342.
Crossref | GoogleScholarGoogle Scholar | open url image1

Markwell J, Osterman JC, Mitchell JL (1995) Calibration of the Minolta SPAD-502 leaf chlorophyll meter. Photosynthesis Research 46, 467–472.
Crossref | GoogleScholarGoogle Scholar | open url image1

Marschner H (1995) ‘Mineral nutrition of higher plants.’ (Academic Press: London)

Masarovicova E, Holubova M (1998) Effects of copper on growth and chlorophyll content of some herbs. Rostlinna Vyroba 44, 261–265. open url image1

Maxwell K, Johnson GN (2000) Chlorophyll fluorescence — a practical guide. Journal of Experimental Botany 51, 659–668.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

McLellan AJ , Prati D , Kaltz O , Schmid B (1997) ‘Structure and analysis of phenotypic and genetic variation in clonal plants.’ (Backhuys Publishers: Leiden)

Neales TF, Incoll LD (1968) The control of leaf photosynthesis rate by the level of assimilate concentration in the leaf: a review of the hypothesis. Botanical Review 34, 107–125. open url image1

Nishitani S, Takada T, Kachi N (1999) Optimal resource allocation to seeds and vegetative propagules under density-dependent regulation in Syneilesis palmate (Compositae). Plant Ecology 141, 179–189.
Crossref | GoogleScholarGoogle Scholar | open url image1

Oborny B , Podani J (1996) ‘The role of clonality in plant communities.’ (Opulus Press: Uppsala)

Outridge PM, Hutchinson TC (1990) Effects of cadmium on ramet integration and resource allocation in the clonal fern Salvinia molesta. Oecologia 84, 215–223. open url image1

Outridge PM, Hutchinson TC (1991) Induction of cadmium tolerance by acclimation transferred between ramets of the clonal fern Salvinia minima Baker. New Phytologist 117, 597–605.
Crossref | GoogleScholarGoogle Scholar | open url image1

Outridge PM, Rauser WE, Hutchinson TC (1991) Changes in metal-binding peptides due to acclimation to cadmium transferred between ramets of Salvinia minima. Oecologia 88, 109–115.
Crossref | GoogleScholarGoogle Scholar | open url image1

Prasad MNV (1997) Trace metals. In ‘Plant ecophysiology’. (Ed. MNV Prasad) pp. 207–250. (John Wiley & Sons: New York)

Price EAC, Marshall C (1999) Clonal plants and environmental heterogeneity. Plant Ecology 141, 3–7.
Crossref | GoogleScholarGoogle Scholar | open url image1

Roiloa SR, Retuerto R (2005) Presence of developing ramets of Fragaria vesca L. increases photochemical efficiency in parent ramets. International Journal of Plant Sciences 166, 795–803.
Crossref | GoogleScholarGoogle Scholar | open url image1

Ross SM (1994) Sources and forms of potentially toxic metals in soil–plant systems. In ‘Toxic metals in soil-plant systems’. (Ed. SM Ross) pp. 3–25. (John Wiley & Sons: Chichester)

Saitoh T, Seiwa K, Nishiwaki A (2002) Importance of physiological integration of dwarf bamboo to persistence in forest understorey: a field experiment. Journal of Ecology 90, 78–85.
Crossref | GoogleScholarGoogle Scholar | open url image1

Salzman AG (1985) Habitat selection in a clonal plant. Science 228, 603–604.
PubMed |
open url image1

Salzman AG, Parker MA (1985) Neighbours ameliorate local salinity stress for a rhizomatous plant in a heterogeneous environment. Oecologia 65, 273–277.
Crossref | GoogleScholarGoogle Scholar | open url image1

Schellner RA, Newell SJ, Solbrig OT (1982) Studies on the population biology of the genus Viola. IV. Spatial pattern of ramets and seedlings in three stoloniferous species. Journal of Ecology 70, 273–290.
Crossref |
open url image1

Slade AJ, Hutchings MJ (1987) An analysis of the costs and benefits of physiological integration between ramets in the clonal perennial herb Glechoma hederacea. Oecologia 73, 425–431.
Crossref | GoogleScholarGoogle Scholar | open url image1

Stuefer JF (1997) Division of labour in clonal plants? PhD Thesis, University of Utrecht.

Stuefer JF, de Kroon H, During HJ (1996) Exploitation of environmental heterogeneity by spatial division of labour in a clonal plant. Functional Ecology 10, 328–334.
Crossref |
open url image1

Subhash N, Mohanan CN, Mallia R, Muralidharan V (2004) Quantification of stress adaptation by laser-induced fluorescence spectroscopy of plants exposed to engine exhaust emission and drought. Functional Plant Biology 31, 709–719.
Crossref | GoogleScholarGoogle Scholar | open url image1

Sweet GB, Wareing PF (1966) Role of plant growth in regulating photosynthesis. Nature 210, 77–79.
Crossref |
open url image1

Turkington R, Harper JL (1979) The growth, distribution and neighbour relationships of Trifolium repens in a permanent pasture. II. Inter-and intra-specific contact. Journal of Ecology 67, 219–230.
Crossref |
open url image1

van Groenendael JM , de Kroon H (1990) ‘Clonal growth in plants: regulation and function.’ (SPB Academic Publishing: The Hague)

Welham CVJ, Turkington R, Sayre C (2002) Morphological plasticity of white clover (Trifolium repens L.) in response to spatial and temporal resource heterogeneity. Oecologia 130, 231–238. open url image1

Wijesinghe DK, Hutchings MJ (1999) The effects of environmental heterogeneity on the performance of Glechoma hederacea: the interactions between patch contrast and patch scale. Journal of Ecology 87, 860–872.
Crossref | GoogleScholarGoogle Scholar | open url image1

Wood CW, Reeves DW, Himelrick DG (1993) Relationships between chlorophyll meter readings and leaf chlorophyll concentration, N status, and crop yield: a review. Proceedings of the Agronomy Society of New Zealand 23, 1–9. open url image1