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

Potential advantages of highly mycotrophic foraging for the establishment of early successional pioneer plants on sand

Ingo Höpfner A B , Martina Friede A , Stephan Unger A and Wolfram Beyschlag A
+ Author Affiliations
- Author Affiliations

A Department of Experimental and Systems Ecology, University of Bielefeld, Universitätsstr. 25, D-33615 Bielefeld, Germany.

B Corresponding author. Email: ingo.hoepfner@uni-bielefeld.de

Functional Plant Biology 42(1) 95-104 https://doi.org/10.1071/FP14097
Submitted: 28 March 2014  Accepted: 11 July 2014   Published: 25 August 2014

Abstract

Adaptive traits ensuring efficient nutrient acquisition, such as extensive fine root systems, are crucial for establishment of pioneer plants on bare sand. Some successful pioneer species of temperate, European sand ecosystems are characterised as obligate mycorrhizals, thus likely substituting fine roots with arbuscular mycorrhizal fungi (AMF). However, it is not clear whether AM fungal-mediated acquisition of scarce and immobile nutrients such as phosphorus (P) is an advantageous strategy on bare sand over foraging via roots. We compared the foraging performance of three obligately mycorrhizal forbs and two facultatively mycorrhizal grasses, regarding the influence of AMF on their capacity to acquire P from bare sand. Comparison of mycorrhizal and non-mycorrhizal individuals revealed a markedly higher AM fungal-dependency for P acquisition and growth in the forbs than in the grasses. Periodical soil core sampling, allowing for assessment of root and hyphal growth rates, revealed hyphal growth to markedly enlarge the total absorptive surface area (SA) in the forbs, but not in the grasses. Correlations between SA growth and P depletion suggest an AM fungal-induced enhanced capacity for rapid soil P exploitation in the forbs. Our study showed that AM fungal-mediated foraging may be an advantageous strategy over root-mediated foraging in sand pioneer plants.

Additional keywords: adaptation, arbuscular mycorrhizas, nutrient deficiency, open sand ecosystems, phosphorus uptake, root growth.


References

Ayres RL, Gange AC, Aplin DM (2006) Interactions between arbuscular mycorrhizal fungi and intraspecific competition affect size, and size inequality, of Plantago lanceolata L. Journal of Ecology 94, 285–294.
Interactions between arbuscular mycorrhizal fungi and intraspecific competition affect size, and size inequality, of Plantago lanceolata L.CrossRef |

Bartelheimer M, Steinlein T, Beyschlag W (2006) Aggregative root placement: a feature during interspecific competition in inland sand-dune habitats. Plant and Soil 280, 101–114.
Aggregative root placement: a feature during interspecific competition in inland sand-dune habitats.CrossRef | 1:CAS:528:DC%2BD28XhslOrs7o%3D&md5=4497d83786487f175b9ffaa3ff9696e6CAS |

Bartelheimer M, Steinlein T, Beyschlag W (2008) 15N-nitrate-labelling demonstrates a size symmetric competitive effect on belowground resource uptake. Plant Ecology 199, 243–253.
15N-nitrate-labelling demonstrates a size symmetric competitive effect on belowground resource uptake.CrossRef |

Baylis GTS (1975) The magnolioid mycorrhiza and mycotrophy in root systems derived from it. In ‘Endomycorrhizas’. (Eds FE Sanders, B Mosse, PB Tinker) pp. 373–389. (Academic Press: New York)

Bishop LA, Davy AJ (1994) Hieracium pilosella L. (Pilosella officinarum F. Schultz & Schultz-Bip.). Journal of Ecology 82, 195–210.
Hieracium pilosella L. (Pilosella officinarum F. Schultz & Schultz-Bip.).CrossRef |

Boorman LA (1982) Some plant growth patterns in relation to the sand dune habitat. Journal of Ecology 70, 607–614.
Some plant growth patterns in relation to the sand dune habitat.CrossRef |

Brundrett MC (2002) Coevolution of roots and mycorrhizas of land plants. New Phytologist 154, 275–304.
Coevolution of roots and mycorrhizas of land plants.CrossRef |

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 and Soil 320, 37–77.
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.CrossRef | 1:CAS:528:DC%2BD1MXmvFGjt7g%3D&md5=e89d9f2fd9370e9e2ed8461e10ccb887CAS |

Casper BB, Jackson RB (1997) Plant competition underground. Annual Review of Ecology and Systematics 28, 545–570.
Plant competition underground.CrossRef |

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 Phytologist 133, 453–460.
Facilitation of plant phosphate acquisition by arbuscular mycorrhizas from enriched soil patches. 1. Roots and hyphae exploiting the same soil volume.CrossRef | 1:CAS:528:DyaK28XlsV2rsL4%3D&md5=acba6b9f430218164a48b256cf19d946CAS |

Ellenberg H (1996) Vegetation Mitteleuropas mit den Alpen. In ‘Okologischer, dynamischer und historischer Sicht’. (5th edn) (Ulmer: Stuttgart, Germany)

Fitter AH (1991) Costs and benefits of mycorrhizas – implications for functioning under natural conditions. Experientia 47, 350–355.
Costs and benefits of mycorrhizas – implications for functioning under natural conditions.CrossRef |

Francis R, Read DJ (1995) Mutualism and antagonism in the mycorrhizal symbiosis, with special reference to impact on plant community structure. Canadian Journal of Botany - Revue Canadienne de Botanique 73, 1301–1309.

Gange AC, Ayres RL (1999) On the relation between arbuscular mycorrhizal colonization and plant ‘benefit’. Oikos 87, 615–621.
On the relation between arbuscular mycorrhizal colonization and plant ‘benefit’.CrossRef |

Grime JP (2006) ‘Plant strategies, vegetation processes, and ecosystem properties.’ (2nd edn) (John Wiley & Sons: Hoboken, NY, USA)

Grime JP, Mackey JM, Hillier SH, Read DJ (1987) Floristic diversity in a model system using experimental microcosms. Nature 328, 420–422.
Floristic diversity in a model system using experimental microcosms.CrossRef |

Harley JL (1989) The significance of mycorrhiza. Mycological Research 92, 129–139.
The significance of mycorrhiza.CrossRef |

Hartnett DC, Wilson GW (2002) The role of mycorrhizas in plant community structure and dynamics: lessons from grasslands. Plant and Soil 244, 319–331.
The role of mycorrhizas in plant community structure and dynamics: lessons from grasslands.CrossRef | 1:CAS:528:DC%2BD38XntFGrtbY%3D&md5=60ef4f1ef8a84951fb3ac4b4068556f0CAS |

Heinemeyer A, Ineson P, Ostle N, Fitter AH (2006) Respiration of the external mycelium in the arbuscular mycorrhizal symbiosis shows strong dependence on recent photosynthates and acclimation to temperature. New Phytologist 171, 159–170.
Respiration of the external mycelium in the arbuscular mycorrhizal symbiosis shows strong dependence on recent photosynthates and acclimation to temperature.CrossRef | 1:CAS:528:DC%2BD28Xnt1Cls7s%3D&md5=a43f2c9575c8776a3de4dbf3646c0eb9CAS | 16771991PubMed |

Hetrick BA, Wilson GW, Cox TS (1992) Mycorrhizal dependence of modern wheat-varieties, landraces, and ancestors. Canadian Journal of Botany – Revue Canadienne de Botanique 70, 2032–2040.

Hetrick BA, Wilson GW, Todd TC (1996) Mycorrhizal response in wheat cultivars: relationship to phosphorus. Canadian Journal of Botany – Revue Canadienne de Botanique 74, 19–25.

Hoagland DR, Arnon I (1950) ‘The water culture method for growing plants without soil.’ (California Agriculture Experiment Station, Berkeley, CA, USA)

Hodge A (2004) The plastic plant: root responses to heterogeneous supplies of nutrients. New Phytologist 162, 9–24.
The plastic plant: root responses to heterogeneous supplies of nutrients.CrossRef |

Hoeksema JD, Chaudhary VB, Gehring CA, Johnson NC, Karst J, Koide RT, Pringle A, Zabinski C, Bever JD, Moore JC, Wilson GW, Klironomos JN, Umbanhowar J (2010) A meta-analysis of context-dependency in plant response to inoculation with mycorrhizal fungi. Ecology Letters 13, 394–407.
A meta-analysis of context-dependency in plant response to inoculation with mycorrhizal fungi.CrossRef | 20100237PubMed |

Jakobsen I, Abbott LK, Robson AD (1992) External hyphae of vesicular-arbuscular mycorrhizal fungi associated with Trifolium subterraneum L. 1. Spread of hyphae and phosphorus inflow into roots. New Phytologist 120, 371–380.
External hyphae of vesicular-arbuscular mycorrhizal fungi associated with Trifolium subterraneum L. 1. Spread of hyphae and phosphorus inflow into roots.CrossRef | 1:CAS:528:DyaK38XisFClu7o%3D&md5=1f3791fe0e6c8c31a1f5a451b0f68cb6CAS |

Janos DP (2007) Plant responsiveness to mycorrhizas differs from dependence upon mycorrhizas. Mycorrhiza 17, 75–91.
Plant responsiveness to mycorrhizas differs from dependence upon mycorrhizas.CrossRef | 17216499PubMed |

Jentsch A, Beyschlag W (2003) Vegetation ecology of dry acidic grasslands in the lowland area of central Europe. Flora 198, 3–25.
Vegetation ecology of dry acidic grasslands in the lowland area of central Europe.CrossRef |

Johnson NC (2010) Resource stoichiometry elucidates the structure and function of arbuscular mycorrhizas across scales. New Phytologist 185, 631–647.
Resource stoichiometry elucidates the structure and function of arbuscular mycorrhizas across scales.CrossRef | 1:CAS:528:DC%2BC3cXitFKnsrs%3D&md5=a8c11e6df61c1593ad51729941d01a35CAS | 19968797PubMed |

Koide RT, Li MG (1989) Appropriate controls for vesicular-arbuscular mycorrhiza research. New Phytologist 111, 35–44.
Appropriate controls for vesicular-arbuscular mycorrhiza research.CrossRef |

Koide RT, Goff MD, Dickie IA (2000) Component growth efficiencies of mycorrhizal and nonmycorrhizal plants. New Phytologist 148, 163–168.
Component growth efficiencies of mycorrhizal and nonmycorrhizal plants.CrossRef |

Kutschera L, Lichtenegger E (1982) ‘Wurzelatlas mitteleuropäischer Grünlandpflanzen. Monocotyledoneae.’ (Verlag: Stuttgart, Germany)

Lambers H, Raven JA, Shaver GR, Smith SE (2008) Plant nutrient-acquisition strategies change with soil age. Trends in Ecology & Evolution 23, 95–103.
Plant nutrient-acquisition strategies change with soil age.CrossRef |

Le Bagousse-Pinguet Y, Forey E, Touzard B, Michalet R (2013) Disentangling the effects of water and nutrients for studying the outcome of plant interactions in sand dune ecosystems. Journal of Vegetation Science 24, 375–383.
Disentangling the effects of water and nutrients for studying the outcome of plant interactions in sand dune ecosystems.CrossRef |

Li XL, George E, Marschner H (1991) Extension of the phosphorus depletion zone in VA-mycorrhizal white clover in a calcareous soil. Plant and Soil 136, 41–48.
Extension of the phosphorus depletion zone in VA-mycorrhizal white clover in a calcareous soil.CrossRef |

McGonigle T, Miller MH, Evans DG, Fairchild GL, Swan JA (1990) A new method which gives an objective-measure of colonization of roots by vesicular arbuscular mycorrhizal fungi. New Phytologist 115, 495–501.
A new method which gives an objective-measure of colonization of roots by vesicular arbuscular mycorrhizal fungi.CrossRef |

Miller RM, Reinhardt DR, Jastrow JD (1995) External hyphal production of vesicular-arbuscular mycorrhizal fungi in pasture and tallgrass prairie communities. Oecologia 103, 17–23.
External hyphal production of vesicular-arbuscular mycorrhizal fungi in pasture and tallgrass prairie communities.CrossRef |

Olff H, Huisman J, van Tooren BF (1993) Species dynamics and nutrient accumulation during early primary succession in coastal sand dunes. Journal of Ecology 81, 693–706.
Species dynamics and nutrient accumulation during early primary succession in coastal sand dunes.CrossRef |

Parádi I, Bratek Z, Láng F (2003) Influence of arbuscular mycorrhiza and phosphorus supply on polyamine content, growth and photosynthesis of Plantago lanceolata. Biologia Plantarum 46, 563–569.
Influence of arbuscular mycorrhiza and phosphorus supply on polyamine content, growth and photosynthesis of Plantago lanceolata.CrossRef |

Phillips JM, Hayman DS (1970) Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Transactions of the British Mycological Society 55, 158–161.
Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection.CrossRef |

Plenchette C, Fortin JA, Furlan V (1983) Growth responses of several plant species to mycorrhizae in a soil of moderate P-fertility.1. Mycorrhizal dependency under field conditions. Plant and Soil 70, 199–209.
Growth responses of several plant species to mycorrhizae in a soil of moderate P-fertility.1. Mycorrhizal dependency under field conditions.CrossRef | 1:CAS:528:DyaL3sXhvFGjur8%3D&md5=421649530a19fdd2b5f7e9f683c1a8afCAS |

Reinhart KO, Wilson GW, Rinella MJ (2012) Predicting plant responses to mycorrhizae: integrating evolutionary history and plant traits. Ecology Letters 15, 689–695.
Predicting plant responses to mycorrhizae: integrating evolutionary history and plant traits.CrossRef | 22507627PubMed |

Richardson AE, Hocking PJ, Simpson RJ, George TS (2009) Plant mechanisms to optimise access to soil phosphorus. Crop and Pasture Science 60, 124–143.
Plant mechanisms to optimise access to soil phosphorus.CrossRef | 1:CAS:528:DC%2BD1MXitlyrs7s%3D&md5=4458819c3cce57f0de8f6bc162bb9769CAS |

Rillig MC, Field CB, Allen MF (1999) Soil biota responses to long-term atmospheric CO2 enrichment in two California annual grasslands. Oecologia 119, 572–577.
Soil biota responses to long-term atmospheric CO2 enrichment in two California annual grasslands.CrossRef |

Ryser P, Lambers H (1995) Root and leaf attributes accounting for the performance of fast- and slow-growing grasses at different nutrient supply. Plant and Soil 170, 251–265.
Root and leaf attributes accounting for the performance of fast- and slow-growing grasses at different nutrient supply.CrossRef | 1:CAS:528:DyaK2MXmtFOmtbs%3D&md5=c30a5f76116ccbcabf913f82fc0f0576CAS |

Schüller H (1969) Die CAL-Methode, eine neue Methode zur Bestimmung des pflanzenverfügbaren Phosphates in Böden. Zeitschrift für Pflanzenernährung und Bodenkunde 123, 48–63.
Die CAL-Methode, eine neue Methode zur Bestimmung des pflanzenverfügbaren Phosphates in Böden.CrossRef |

Schultz PA, Miller RM, Jastrow JD, Rivetta CV, Bever JD (2001) Evidence of a mycorrhizal mechanism for the adaptation of Andropogon gerardii (Poaceae) to high- and low-nutrient prairies. American Journal of Botany 88, 1650–1656.
Evidence of a mycorrhizal mechanism for the adaptation of Andropogon gerardii (Poaceae) to high- and low-nutrient prairies.CrossRef | 1:STN:280:DC%2BC3Mngt1artg%3D%3D&md5=b1599349f194e63617c6af464d29680bCAS | 21669699PubMed |

Schweiger PF, Robson AD, Barrow NJ (1995) Root hair length determines beneficial effect of a Glomus species on shoot growth of some pasture species. New Phytologist 131, 247–254.
Root hair length determines beneficial effect of a Glomus species on shoot growth of some pasture species.CrossRef |

Seifert EK, Bever JD, Maron JL (2009) Evidence for the evolution of reduced mycorrhizal dependence during plant invasion. Ecology 90, 1055–1062.
Evidence for the evolution of reduced mycorrhizal dependence during plant invasion.CrossRef | 19449699PubMed |

Smith SE, Read DJ (2008) ‘Mycorrhizal symbiosis.’ (3rd edn) (Academic Press: London)

Smith SE, Smith FA, Jakobsen I (2003) Mycorrhizal fungi can dominate phosphate supply to plants irrespective of growth responses. Plant Physiology 133, 16–20.
Mycorrhizal fungi can dominate phosphate supply to plants irrespective of growth responses.CrossRef | 1:CAS:528:DC%2BD3sXntlait7o%3D&md5=b06c832d79aaaa0bb51f42cf3cefc210CAS | 12970469PubMed |

Süß K, Storm C, Zehm A, Schwabe A (2004) Succession in inland sand ecosystems: which factors determine the occurrence of the tall grass species Calamagrostis epigejos (L.) Roth and Stipa capillata L.? Plant Biology 6, 465–476.
Succession in inland sand ecosystems: which factors determine the occurrence of the tall grass species Calamagrostis epigejos (L.) Roth and Stipa capillata L.?CrossRef | 15248130PubMed |

Tilman D (1985) The resource-ratio hypothesis of plant succession. American Naturalist 125, 827–852.
The resource-ratio hypothesis of plant succession.CrossRef |

Titus JH, del Moral R (1998) Vesicular-arbuscular mycorrhizae influence Mount St Helens pioneer species in greenhouse experiments. Oikos 81, 495–510.
Vesicular-arbuscular mycorrhizae influence Mount St Helens pioneer species in greenhouse experiments.CrossRef |

van der Heijden MG, Horton TR (2009) Socialism in soil? The importance of mycorrhizal fungal networks for facilitation in natural ecosystems. Journal of Ecology 97, 1139–1150.
Socialism in soil? The importance of mycorrhizal fungal networks for facilitation in natural ecosystems.CrossRef |

van der Heijden MG, Boller T, Wiemken A, Sanders IR (1998) Different arbuscular mycorrhizal fungal species are potential determinants of plant community structure. Ecology 79, 2082–2091.
Different arbuscular mycorrhizal fungal species are potential determinants of plant community structure.CrossRef |

Vance CP, Uhde-Stone C, Allan DL (2003) Phosphorus acquisition and use: critical adaptations by plants for securing a nonrenewable resource. New Phytologist 157, 423–447.
Phosphorus acquisition and use: critical adaptations by plants for securing a nonrenewable resource.CrossRef | 1:CAS:528:DC%2BD3sXisF2gu70%3D&md5=63c30bc4fff8385ad5dbf53a2f613d58CAS |

Wang B, Qiu Y (2006) Phylogenetic distribution and evolution of mycorrhizas in land plants. Mycorrhiza 16, 299–363.
Phylogenetic distribution and evolution of mycorrhizas in land plants.CrossRef | 1:STN:280:DC%2BD28vit1OltA%3D%3D&md5=465a07ab5af4e88070cfbb705937b708CAS | 16845554PubMed |

Watanabe FS, Olsen SR (1965) Test of an ascorbic acid method for determining phosphorus in water and NaHCO3 extracts from soils. Soil Science Society of America Journal 29, 677–678.
Test of an ascorbic acid method for determining phosphorus in water and NaHCO3 extracts from soils.CrossRef | 1:CAS:528:DyaF28XovVahsA%3D%3D&md5=2b7c8b2002d163f48835b87119d66b9fCAS |

Weigelt A, Steinlein T, Beyschlag W (2005) Competition among three dune species: the impact of water availability on below-ground processes. Plant Ecology 176, 57–68.
Competition among three dune species: the impact of water availability on below-ground processes.CrossRef |

Weigelt A, Schumacher J, Walther T, Bartelheimer M, Steinlein T, Beyschlag W (2007) Identifying mechanisms of competition in multi-species communities. Journal of Ecology 95, 53–64.
Identifying mechanisms of competition in multi-species communities.CrossRef |



Rent Article (via Deepdyve) Export Citation Cited By (8)