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Restoring native forest ecosystems after exotic tree plantation in Madagascar: combination of the local ectotrophic species Leptolena bojeriana and Uapaca bojeri mitigates the negative influence of the exotic species Eucalyptus camaldulensis and Pinus patula

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Abstract

The objectives of this study were to determine the impact of two exotic tree species (pine and eucalypts) on the early growth of Uapaca bojeri (an endemic tree species from Madagascar) via their influence on soil chemical, microbial characteristics, on ectomycorrhizal fungal community structures in a Madagascarian highland forest and to test the ability of an early-successional ectomycorrhizal shrub, Leptolena bojeriana, to mitigate the impacts of these exotic species. Finally, we hypothesized that L. bojeriana could act as a natural provider for ectomycorrhizal propagules. Soil bioassays were conducted with U. bojeri seedlings grown in soils collected under the native tree species (U. bojeri and L. bojeriana) and two exotic tree species (Eucalyptus camaldulensis and Pinus patula) and in the same soils but previously cultured by L. bojeriana seedlings. This study clearly shows that (1) the introduction of exotic tree species induces significant changes in soil biotic and abiotic characteristics, (2) exotic-invaded soil significantly reduces the early growth and ectomycorrhization of U. bojeri seedlings and (3) L. bojeriana decreased these negative effects of the exotic tree species by facilitating ectomycorrhizal establishment and consequently improved the U. bojeri early growth. This study provides evidence that L. bojeriana can facilitate the ectomycorrhizal infection of U. bojeri and mitigates the negative effects of the introduction of exotic tree species on the early growth of the native tree species. From a practical point of view, the use of ectotrophic early-successional shrub species should be considered to improve forest resaturation after exotic invasion.

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References

  • Acosta-Martinez V, Tabatai MA (2000) Enzyme activities in a limed agricultural soil. Biol Fert Soil 31:85–91

    Article  CAS  Google Scholar 

  • Agerer R (1987–1996) Colour atlas of ectomycorrhizae. Einhorn-Verlag Eduard Dietenberger, Schwäbisch Gmünd

  • Agerer R (1995) Anatomical characteristics of identified ectomycorrhizas: an attempt towards a natural classification. In: Varma A, Hock B (eds) Mycorrhiza: structure, function, molecular biology and biotechnology. Springer, Berlin, pp 687–734

    Google Scholar 

  • Alef K (1998) Estimation of the hydrolysis of fluorescein diacetate. In: Alef K, Nannipieri P (eds) Methods in applied soil microbiology and biochemistry. Academic Press, London, pp 232–233

    Google Scholar 

  • Allen MF (1987) Re-establishment of mycorrhizas on Mount St Helens: migration vectors. Trans Br Mycol Soc 88:413–417

    Article  Google Scholar 

  • Ashton IW, Hyatt LA, Howe KM, Gurevitch J, Lerdau MT (2005) Invasive species accelerate decomposition and litter nitrogen loss in a mixed deciduous forest. Ecol Appl 15:1263–1272

    Article  Google Scholar 

  • Aubert G (1978) Méthodes d’Analyse des sols. Edition CRDP, Marseille, p 360

    Google Scholar 

  • Batten K, Scow K, Davies K, Harrison S (2006) Two invasive plants alter soil microbial community composition in serpentine grasslands. Biol Invasions 8:217–230

    Article  Google Scholar 

  • Baxter JW, Dighton J (2001) Ectomycorrhizal diversity alters growth and nutrient acquisition of grey birch (Betula populifolia) seedlings in host-symbiont culture conditions. New Phytol 152:139–149

    Article  Google Scholar 

  • Brundrett MC (1991) Mycorrhizas in natural ecosystems. In: Macfayden A, Begon M, Fitter AH (eds) Advances in ecological research, vol 21. Academic Press, London, pp 171–313

    Google Scholar 

  • Callaway RM, Pennings SC (2000) Facilitation may buffer competitive effects: indirect and diffuse interactions among salt marsh plants. Am Nat 156:416–424

    Article  Google Scholar 

  • Callaway RM, Ridenour WM (2004) Novel weapons: invasive success and the evolution of increased competitive ability. Front Ecol Environ 2:436–443

    Article  Google Scholar 

  • del Moral R, Muller CH (1970) The allelopathic effects of Eucalyptus camaldulensis. Am Midl Nat 83:254–282

    Article  Google Scholar 

  • Dickie IA, Reich PB (2005) Ectomycorrhizal fungal communities at forest edges. J Ecol 93:244–255

    Article  Google Scholar 

  • Dickie IA, Koide RT, Steiner KC (2002) Influence of established trees on mycorrhizas, growth and nutrition of Quercus rubra seedlings. Ecol Monogr 72:505–521

    Article  Google Scholar 

  • Dickie IA, Guza RC, Krasewski SE, Reich PB (2004) Shared ectomycorrhizal fungi between a herbaceous perennial (Helianthemum bicknellii) and oak (Quercus) seedlings. New Phytol 164:375–382

    Article  Google Scholar 

  • Diédhiou AG, Selosse M-A, Galiana A, Diabaté M, Dreyfus B, Bâ AM, de Faria SM, Béna G (2010) Multi-host ectomycorrhizal fungi are predominant in a Guinean tropical rainforest and shared between canopy trees and seedlings. Environ Microbiol 12:2219–2232

    PubMed  Google Scholar 

  • Dray S, Dufour AB (2007) The ade4 package: implementing the duality diagram for ecologists. J Stat Soft 22:1–20

    Google Scholar 

  • Ducousso M, Bourgeois C, Buyck B, Eyssartier G, Vincelette M, Rabevohitra R, Béna G, Randrihasipara L, Dreyfus B, Prin Y (2004) The last common ancestor of Sarcolaenaceae and Asian dipterocarp trees was ectomycorrhizal before the India-Madagascar separation, about 88 million years ago. Mol Ecol 13:231–236

    Article  PubMed  CAS  Google Scholar 

  • Duponnois R, Plenchette C, Prin Y, Ducousso M, Kisa M, Bâ AM, Galiana A (2007) Use of mycorrhizal inoculation to improve reafforestation process with Australian Acacia in Sahelian ecozones. Ecol Eng 29:105–112

    Article  Google Scholar 

  • Ehrenfeld JG, Kourtev PS, Huang WS (2001) Changes in soil functions following invasions of exotic understory plants in deciduous forests. Ecol Appl 11:1287–1300

    Article  Google Scholar 

  • Faye A, Krasova-Wade T, Thiao M, Thioulouse J, Neyra M, Prin Y, Galiana A, Ndoye I, Dreyfus B, Duponnois R (2009) Controlled ectomycorrhization of an exotic legume tree species Acacia holosericea affects the structure of root nodule bacteria community and their symbiotic effectiveness on Faidherbia albida, a native Sahelian Acacia. Soil Biol Biochem 41:1245–1252

    Article  CAS  Google Scholar 

  • Franco AC, Nobel PS (1988) Interactions between seedlings of Agave deserti and the nurse plant Hilaria rigida. Ecology 69:1731–1740

    Article  Google Scholar 

  • Gade DW (1996) Deforestation and its effects in highland Madagascar. Mt Res Dev 16:101–116

    Article  Google Scholar 

  • Hawkes CV, Wren IF, Herman DJ, Firestone MK (2005) Plant invasion alters nitrogen cycling by modifying the soil nitrifying community. Ecol Lett 8:976–985

    Article  Google Scholar 

  • Janos DP (1980) Vesicular-arbuscular mycorrhizae affect lowland tropical rain forest plant growth. Ecology 61:151–162

    Article  Google Scholar 

  • Janos DP (1996) Mycorrhizas, succession and rehabilitation of deforested lands in the humid tropics. In: Frankland JC, Magan N, Gadd GM (eds) Fungi and environment change. Cambridge University Press, Cambridge, pp 129–161

    Chapter  Google Scholar 

  • Johansson JF, Paul LR, Finlay RD (2004) Microbial interactions in the mycorrhizosphere and their significance for sustainable agriculture. FEMS Microbiol Ecol 48:1–13

    Article  PubMed  CAS  Google Scholar 

  • John MK (1970) Colorimetric determination in soil and plant material with ascorbic acid. Soil Sci 68:171–177

    Google Scholar 

  • Jones MD, Durall DM, Cairney JWG (2003) Ectomycorrhizal fungal communities in young forest stands regenerating after clearcut logging. New Phytol 157:399–422

    Article  Google Scholar 

  • Jonsson L, Dahlberg A, Nilsson MC, Karen O, Zackrisson O (1999) Continuity of ectomycorrhizal fungi in self-regenerating boreal Pinus sylvestris forests studied by comparing mycobiont diversity on seedlings and mature trees. New Phytol 142:151–162

    Article  Google Scholar 

  • Kisa M, Sanon A, Thioulouse J, Assigbetse K, Sylla S, Spichiger R, Dieng L, Berthelin J, Prin Y, Galiana A, Lepage M, Duponnois R (2007) Arbuscular mycorrhizal symbiosis can counterbalance the negative influence of the exotic tree species Eucalyptus camaldulensis on the structure and functioning of soil microbial communities in a Sahelian soil. FEMS Microbiol Ecol 62:32–44

    Article  PubMed  CAS  Google Scholar 

  • Kivlin SN, Hawkes CV (2011) Differentiating between effects of invasion and diversity: impacts of aboveground plant communities on belowground fungal communities. New Phytol 189:526–535

    Article  PubMed  Google Scholar 

  • Kourtev PS, Huang WZ, Ehrenfeld JG (1999) Differences in earthworm densities and nitrogen dynamics in soils under exotic and native plant species. Biol Invasions 1:237–245

    Article  Google Scholar 

  • Kourtev PS, Ehrenfeld JG, Häggblom M (2002) Exotic plant species alter the microbial community structure and function in the soil. Ecology 83:3152–3166

    Article  Google Scholar 

  • Krämer S, Green DM (2000) Acid and alkaline phosphatase dynamics and their relationship to soil microclimate in a semiarid woodland. Soil Biol Biochem 32:179–188

    Article  Google Scholar 

  • Liancourt P, Callaway RM, Michalet R (2005) Stress tolerance and competitive-response ability determine the outcome of biotic interactions. Ecology 86:1611–1618

    Article  Google Scholar 

  • Lilleskov EA, Hobbie EA, Fahey TJ (2002) Ecto- mycorrhizal fungal taxa differing in response to nitrogen deposition also differ in pure culture organic nitrogen use and natural abundance of nitrogen isotopes. New Phytol 154:219–231

    Article  CAS  Google Scholar 

  • Marx DH (1991) The practical significance of ectomycorrhizae in forest establishment. Ecophysiology of ectomycorrhizaeof forest trees, Marcus Wallenberg Foundation Symposia proceedings 7:54–90

  • Matsuda Y, Hijii N (2004) Ectomycorrhizal fungal communities in an Abies firma forest, with special reference to ectomycorrhizal associations between seedlings and mature trees. Can J Bot 82:822–829

    Article  Google Scholar 

  • Mikola P (1970) Mycorrhizal inoculation in afforestation. Int Rev For Res 3:123–196

    Google Scholar 

  • Nara K (2005) Ectomycorrhizal networks and seedling establishment during early primary succession. New Phytol 169:169–178

    Article  Google Scholar 

  • Newman EI (1988) Mycorrhizal links between plants: their functioning and ecological significance. Adv Ecol Res 18:243–270

    Article  Google Scholar 

  • Nicholas KB, Nicholas HB (1997) Genedoc: a toll for editing and annotating multiple sequence alignments. Distributed by the authors

  • Niering WA, Whittaker RH, Lowe CH (1963) The saguaro: a population in relation to environment. Science 142:15–23

    Article  PubMed  CAS  Google Scholar 

  • Olsen SR, Cole CV, Watanabe FS, Dean LA (1954) Estimation of available phosphorus in soils by extraction with sodium bicarbonate. Circular, vol 939. US Department of Agriculture, Washington, DC, p 19

  • Onguene NA, Kuyper TW (2002) Importance of the ectomycorrhizal network for seedling survival and ectomycorrhiza formation in rain forests of south Cameroon. Mycorrhiza 12:13–17

    Article  PubMed  CAS  Google Scholar 

  • Ouahmane L, Hafidi M, Kisa M, Boumezzough A, Thioulouse J, Plenchette C, Duponnois R (2006) Some Mediterranean plant species (Lavandula spp. and Thymus satureioides) act as “plant nurses” for the early growth of Cupressus atlantica. Plant Ecol 185:123–134

    Article  Google Scholar 

  • Parrot A (1925) Le reboisement de Madagascar par le moyen des forêts de “fokon olona”. Bulletin Economique (Antananarivo) 1–2:55–57

  • Phillips JM, Hayman DS (1970) Improved procedures for clearing and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Trans Br Mycol Soc 55:158–160

    Article  Google Scholar 

  • R Development Core Team (2010) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN: 3-900051-07-0. http://www.R-project.org/

  • Reader RJ, Jalili A, Grime JP, Spencer RE, Matthews N (1992) A comparative study of plasticity in seedling rooting depth in drying soil. J Ecol 81:543–550

    Google Scholar 

  • Rejmanek M (2000) Invasive plants: approaches and predictions. Aust Ecol 25:497–506

    Article  Google Scholar 

  • Remigi P, Faye A, Kane A, Deruaz M, Thioulouse J, Cissoko M, Prin Y, Galiana A, Dreyfus B, Duponnois R (2008) The exotic legume tree species Acacia holosericea alters microbial soil functionalities and the structure of the arbuscular mycorrhizal community. Appl Environ Microb 74:1485–1493

    Article  CAS  Google Scholar 

  • Rivière T, Natarajan K, Dreyfus B (2005) Spatial distribution of ectomycorrhizal Basidiomycete Russula subsect. Foetentinae populations in a primary dipterocarp rainforest. Mycorrhiza 16:143–148

    Article  PubMed  Google Scholar 

  • Rivière T, Diedhiou AG, Diabaté M, Senthilarasu G, Natarajan K, Ducousso M, Verbeken A, Buyck B, Dreyfus B, Bena G, Ba AM (2006) Diversity of ectomycorrhizal Basidiomycetes in West African and Indian tropical rain forests. Mycorrhiza 17:415–428

    Article  Google Scholar 

  • Scarano FR (2002) Structure, function and floristic relationships of plant communities in stressful habitats marginal to the Brazilian Atlantic Rainforest. Ann Bot 90:517–524

    Article  PubMed  Google Scholar 

  • Schinner F, Ohlinger R, Kandeler E, Margesin R (1996) Methods in soil biology. Springer, Berlin

    Book  Google Scholar 

  • Schreiner RP, Mihara KL, Mc Danield H, Benthlenfalvay GJ (2003) Mycorrhizal fungi influence plant and soil functions and interactions. Plant Soil 188:199–209

    Article  Google Scholar 

  • Sicardi M, Garcia-Prechac F, Frioni L (2004) Soil microbial indicators sensitive to land use conversion from pastures to commercial Eucalyptus grandis (Hill ex Maiden) plantations in Uruguay. Appl Soil Ecol 27:125–133

    Article  Google Scholar 

  • Simard SW, Perry DA, Jones MD, Myrold DD, Durall DM, Molina R (1997) Netb transfer of carbon between ectomycorrhizal tree species in the field. Nature 388:579–582

    Article  CAS  Google Scholar 

  • Smith S, Read J (2008) Mycorrhizal symbiosis, 3rd edn. Academic Press, London, p 800

    Google Scholar 

  • Smith OH, Petersen GW, Needelman BA (2000) Environmental indicators of agroecosystems. Adv Agron 69:75–97

    Article  CAS  Google Scholar 

  • Styger E, Rakotondramasy HM, Pfeffer MJ, Fernandes ECM, Bates DM (2007) Influence of slash-and-burn farming practices on fallow succession and land degradation in the rainforest region of Madagascar. Agric Ecosyst Environ 119:257–269

    Article  Google Scholar 

  • Tedersoo L, Suvi T, Beaver K, Koljalg U (2007) Ectomycorrhizal fungi of the Seychelles: diversity patterns and host shifts from the native Vateriopsis seychellarum (Dipterocarpaceae) and Intsia bijuga (Caesalpiniaceae) to the introduced Eucalyptus robusta (Myrtaceae), but not Pinus caribaea. New Phytol 175:321–333

    Article  PubMed  CAS  Google Scholar 

  • Terwilliger J, Pastor J (1999) Small mammals, ectomycorrhizae, and conifer succession in beaver meadows. Oikos 85:83–94

    Article  Google Scholar 

  • Thébaud C, Simberloff D (2001) Are plants really larger in their introduced ranges? Am Nat 157:231–236

    Article  PubMed  Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucl Acids Res 24:4876–4882

    Article  Google Scholar 

  • White TJ, Burns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and applications. Academic Press, San Diego, pp 315–322

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Baohanta, R., Thioulouse, J., Ramanankierana, H. et al. Restoring native forest ecosystems after exotic tree plantation in Madagascar: combination of the local ectotrophic species Leptolena bojeriana and Uapaca bojeri mitigates the negative influence of the exotic species Eucalyptus camaldulensis and Pinus patula . Biol Invasions 14, 2407–2421 (2012). https://doi.org/10.1007/s10530-012-0238-5

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