Abstract
Context-dependent foraging behaviour is acknowledged and well documented for a diversity of animals and conditions. The contextual determinants of plant foraging behaviour, however, are poorly understood. Plant roots encounter patchy distributions of nutrients and soil fungi. Both of these features affect root form and function, but how they interact to affect foraging behaviour is unknown. We extend the use of the marginal value theorem to make predictions about the foraging behaviour of roots, and test our predictions by manipulating soil resource distribution and inoculation by soil fungi. We measured plant movement as both distance roots travelled and time taken to grow through nutrient patches of varied quality. To do this, we grew Achillea millefolium in the centers of modified pots with a high-nutrient patch and a low-nutrient patch on either side of the plant (heterogeneous) or patch-free conditions (homogeneous). Fungal inoculation, but not resource distribution, altered the time it took roots to reach nutrient patches. When in nutrient patches, root growth decreased relative to homogeneous soils. However, this change in foraging behaviour was not contingent upon patch quality or fungal inoculation. Root system breadth was larger in homogeneous than in heterogeneous soils, until measures were influenced by pot edges. Overall, we find that root foraging behaviour is modified by resource heterogeneity but not fungal inoculation. We find support for predictions of the marginal value theorem that organisms travel faster through low-quality than through high-quality environments, with the caveat that roots respond to nutrient patches per se rather than the quality of those patches.
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References
Allison VJ (2002) Nutrients, arbuscular mycorrhizas and competition interact to influence seed production and germination success in Achillea millefolium. Funct Ecol 16:742–749
Augspurger CK (1983) Seed dispersal of the tropical tree, Platypodium-elegans, and the escape of its seedlings from fungal pathogens. J Ecol 71:759–771
Barber I, Huntingford FA (1996) Parasite infection alters schooling behaviour: deviant positioning of helminth-infected minnows in conspecific groups. Proc R Soc Lond B Biol Sci 263:1095–1102
Barber I, Hoare D, Krause J (2000) Effects of parasites on fish behaviour: a review and evolutionary perspective. Rev Fish Biol Fish 10:131–165
Bever JD, Dickie IA, Facelli E, Facelli JM, Klironomos J, Moora M, Rillig MC, Stock WD, Tibbett M, Zobel M (2010) Rooting theories of plant community ecology in microbial interactions. Trends Ecol Evol 25:468–478
Brown JS, Kotler BP (2004) Hazardous duty pay and the foraging cost of predation. Ecol Lett 7:999–1014
Brundrett MC (2009) Mycorrhizal associations and other means of nutrition of vascular plants: understanding the global diversity of host plants by resolving conflicting information and developing reliable means of diagnosis. Plant Soil 320:37–77
Cahill JF, McNickle GG (2011) The behavioural ecology of nutrient foraging by plants. Annu Rev Ecol Evol Systemat 42:289–311
Cahill JF, McNickle GG, Haag JJ, Lamb EG, Nyanumba SM, Clair CCS (2010) Plants integrate information about nutrients and neighbours. Science 328:1657
Cain ML (1994) Consequences of foraging in clonal plant-species. Ecology 75:933–944
Carvalho LM, Correia PM, Ryel RJ, Martins-Loucao MA (2003) Spatial variability of arbuscular mycorrhizal fungal spores in two natural plant communities. Plant Soil 251:227–236
Charnov EL (1976) Optimal foraging, marginal value theorem. Theor Popul Biol 9:129–136
Cuevas-Reyes P, Fernandes GW, Gonzalez-Rodriguez A, Pimenta M (2011) Effects of generalist and specialist parasitic plants (Loranthaceae) on the fluctuating asymmetry patterns of ruprestrian host plants. Basic Appl Ecol 12:449–455
Cui M, Caldwell MM (1996) Facilitation of plant phosphate acquisition by arbuscular mycorrhizas from enriched soil patches. 1. Roots and hyphae exploiting the same soil volume. New Phytol 133:453–460
de Kroon H, Mommer L (2006) Root foraging theory put to the test. Trends Ecol Evol 21:113–116
Farley RA, Fitter AH (1999) Temporal and spatial variation in soil resources in a deciduous woodland. J Ecol 87:688–696
Forde BG (2009) Is it good noise? The role of developmental instability in the shaping of a root system. J Exp Bot 60:3989–4002
Gleeson SK, Fry JE (1997) Root proliferation and marginal patch value. Oikos 79:387–393
Gordon DM (2011) The fusion of behavioural ecology and ecology. Behav Ecol 22:225–230
Grimoldi AA, Kavanova M, Lattanzi FA, Schaufele R, Schnyder H (2006) Arbuscular mycorrhizal colonization on carbon economy in perennial ryegrass: quantification by (CO2)-C-13/(CO2)-C-12 steady-state labelling and gas exchange. New Phytol 172:544–553
Hodge A (2004) The plastic plant: root responses to heterogeneous supplies of nutrients. New Phytol 162:9–24
Hodge A, Robinson D, Fitter AH (2000) An arbuscular mycorrhizal inoculum enhances root proliferation in, but not nitrogen capture from, nutrient-rich patches in soil. New Phytol 145:575–584
Hodge A, Helgason T, Fitter AH (2010) Nutritional ecology of arbuscular mycorrhizal fungi. Fungal Ecol 3:267–273
Hoeksema JD, Chaudhary VB, Gehring CA, Johnson NC, Karst J, Koide RT, Pringle A, Zabinski C, Bever JD, Moore JC, Wilson GWT, Klironomos JN, Umbanhowar J (2010) A meta-analysis of context-dependency in plant response to inoculation with mycorrhizal fungi. Ecol Lett 13:394–407
Jackson RB, Caldwell MM (1993) The scale of nutrient heterogeneity around individual plants and its quantification with geostatistics. Ecology 74:612–614
Jenkins W (1964) A rapid centrifugal-flotation technique for separating nematodes from soil. Plant Disease Report 73:288–300
Jensen EL, Dill LM, Cahill JE (2011) Applying behavioural-ecological theory to plant defence: light-dependent movement in Mimosa pudica suggests a trade-off between predation risk and energetic reward. Am Nat 177:377–381
Johnson HA, Biondini ME (2001) Root morphological plasticity and nitrogen uptake of 59 plant species from the Great Plains grasslands, USA. Basic Appl Ecol 2:127–143
Johnson NC, Graham JH, Smith FA (1997) Functioning of mycorrhizal associations along the mutualism-parasitism continuum. New Phytol 135:575–586
Jones MD, Smith SE (2004) Exploring functional definitions of mycorrhizas: are mycorrhizas always mutualisms? Can J Bot 82:1089–1109
Karban R (2008) Plant behaviour and communication. Ecol Lett 11:727–739
Kelly CK (1990) Plant foraging—a marginal value model and coiling response in Cuscuta-subinclusa. Ecology 71:1916–1925
Klironomos JN (2003) Variation in plant response to native and exotic arbuscular mycorrhizal fungi. Ecology 84:2292–2301
Klironomos JN, Rillig MC, Allen MF (1999) Designing belowground field experiments with the help of semi-variance and power analyses. Appl Soil Ecol 12:227–238
Lamb EG, Haag JJ, Cahill JF (2004) Patch-background contrast and patch density have limited effects on root proliferation and plant performance in Abutilon theophrasti. Funct Ecol 18:836–843
Lefevre T, Lebarbenchon C, Gauthier-Clerc M, Misse D, Poulin R, Thomas F (2009) The ecological significance of manipulative parasites. Trends Ecol Evol 24:41–48
Lempa K, Martel J, Koricheva J, Haukioja E, Ossipov V, Ossipova S, Pihlaja K (2000) Covariation of fluctuating asymmetry, herbivory and chemistry during birch leaf expansion. Oecologia 122:354–360
Levri EP, Lively CM (1996) The effects of size, reproductive condition, and parasitism on foraging behaviour in a freshwater snail, Potamopyrgus antipodarum. Anim Behav 51:891–901
McNickle GG, Cahill JF (2009) Plant root growth and the marginal value theorem. Proc Natl Acad Sci USA 106:4747–4751
McNickle GG, St Clair CC, Cahill JF (2009) Focusing the metaphor: plant root foraging behaviour. Trends Ecol Evol 24:419–426
Moore J (1995) The behaviour of parasitized animals. Bioscience 45:89–96
Moore J (2002) Parasites and the behaviour of animals. Oxford University Press, New York
Mummey DL, Rillig MC (2008) Spatial characterization of arbuscular mycorrhizal fungal molecular diversity at the submetre scale in a temperate grassland. FEMS Microbiol Ecol 64:260–270
Packer A, Clay K (2000) Soil pathogens and spatial patterns of seedling mortality in a temperate tree. Nature 404:278–281
Palmer AR (1996) Waltzing with asymmetry. Bioscience 46:518–532
Rajaniemi TK (2007) Root foraging traits and competitive ability in heterogeneous soils. Oecologia 153:145–152
Raveh A, Kotler BP, Abramsky Z, Krasnov BR (2011) Driven to distraction: detecting the hidden costs of flea parasitism through foraging behaviour in gerbils. Ecol Lett 14:47–51
Smilauer P, Smilauerova M (2000) Effect of AM symbiosis exclusion on grassland community composition. Folia Geobot 35:13–25
Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Academic, London
Stevens GN, Jones RH (2006) Patterns in soil fertility and root herbivory interact to influence fine-root dynamics. Ecology 87:616–624
Stoll P, Schmid B (1998) Plant foraging and dynamic competition between branches of Pinus sylvestris in contrasting light environments. J Ecol 86:934–945
Tibbett M (2000) Roots, foraging and the exploitation of soil nutrient patches: the role of mycorrhizal symbiosis. Funct Ecol 14:397–399
Wijesinghe DK, John EA, Beurskens S, Hutchings MJ (2001) Root system size and precision in nutrient foraging: responses to spatial pattern of nutrient supply in six herbaceous species. J Ecol 89:972–983
Acknowledgments
We thank Tan Bao, Gordon McNickle, Samson Nyanumba, and Shannon White for critical discussions and readings of the manuscript. Justine D. Karst was supported by an Izaak Walton Killam postdoctoral fellowship, Jonathan A. Bennett by a Natural Sciences and Engineering Research Council of Canada postgraduate scholarship, and James F. Cahill by a Natural Sciences and Engineering Research Council of Canada discovery grant and an accelerator supplemental grant. This experiment was conducted in AB, Canada, and complied with all current provincial and federal laws.
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The authors declare that they have no conflict of interest.
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Communicated by Bernhard Schmid.
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Karst, J.D., Belter, P.R., Bennett, J.A. et al. Context dependence in foraging behaviour of Achillea millefolium . Oecologia 170, 925–933 (2012). https://doi.org/10.1007/s00442-012-2358-0
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DOI: https://doi.org/10.1007/s00442-012-2358-0