Abstract
The black truffle (Tuber melanosporum Vittad.) and the summer truffle (Tuber aestivum Vittad.) are two of the most appreciated edible fungi worldwide. The natural distributions of both species partially overlap. However, the interspecific interactions between these truffles and how irrigation and mulching techniques impact the dynamics between them are still unknown. Here, an experimental truffle plantation with Quercus ilex was established in Maials (Catalonia, Spain), combining three soil mulch treatments (white mulch, black mulch and bare soil as a control) and two irrigation regimes (irrigated and non-irrigated as a control) to investigate truffle mycelial dynamics in soil when both truffle species co-occur. The development of truffle mycelium in two different seasons (spring and autumn) in two consecutive years (2017 and 2018) was quantified using qPCR. Truffle mycelia of both species showed greatest development under white mulch. When mycelia of both truffle species co-occurred in soil, irrigation combined with white mulch resulted in greater quantities of T. melanosporum mycelial biomass, whereas the control irrigation treatment favoured the development of T. aestivum. Mulch treatments were also advantageous for seedling growth, which was expressed as root collar diameter and its increment during the study period. Significant relationships between root collar diameter and root growth and the amount of mycelial biomass in the soil were observed for both truffle species. Our results indicate the potential advantages of using white mulch to support irrigation in truffle plantations located in areas with dry Mediterranean climatic conditions to promote the development of Tuber mycelium.
Similar content being viewed by others
References
Baldrian P, Větrovský T, Cajthaml T, Dobiášová P, Petránková M, Šnajdr J, Eichlerová I (2013) Estimation of fungal biomass in forest litter and soil. Fungal Ecol 6:1–11. https://doi.org/10.1016/j.funeco.2012.10.002
Bandopadhyay S, Martin-Closas L, Pelacho AM, DeBruyn JM (2018) Biodegradable plastic mulch films: impacts on soil microbial communities and ecosystem functions. Front Microbiol 9:1–7. https://doi.org/10.3389/fmicb.2018.00819
Baragatti M, Grollemund PM, Montpied P, Dupouey JL, Gravier J, Murat C, Le Tacon F (2019) Influence of annual climatic variations, climate changes, and sociological factors on the production of the Périgord black truffle (Tuber melanosporum Vittad.) from 1903–1904 to 1988–1989 in the Vaucluse (France). Mycorrhiza 29:113–125. https://doi.org/10.1007/s00572-018-0877-1
Bescansa P, Imaz MJ, Virto I, Enrique A, Hoogmoed WB (2006) Soil water retention as affected by tillage and residue management in semiarid Spain. Soil Tillage Res 87(1):19–27. https://doi.org/10.1016/j.still.2005.02.028
Bonet JA, Colinas C (1999) Truficultura, una alternativa rentable para las zonas de media montaña. Rev Desarro Rural y Coop Agrar 153–162
Bonet JA, Fisher CR, Colinas C (2006) Cultivation of black truffle to promote reforestation and land-use stability. Agron Sustain Dev 26(1):69–76. https://doi.org/10.1051/agro
Bonet JA, Oliach D, Fischer CR, Olivera C, Martínez de Aragón J, Colinas C (2009) Cultivation methods of the black truffle the most profitable mediterranean non-wood forest product; a state of the art review. In: Palahí M, Birot Y, Bravo F, Gorriz E (eds.) Modelling, valuing and managing Mediterranean forest ecosystems for non timber goods and services. EFI Proceedings. EFI Joensuu, Joensuu, pp 57–71
Büntgen U, Tegel W, Egli S, Stobbe U, Sproll L, Stenseth NC (2011) Truffles and climate change. Front Ecol Environ 9:150–151. https://doi.org/10.1890/11.WB.004
Büntgen U, Egli S, Camarero JJ, Fischer EM, Stobbe U, Kauserud H, Tegel W, Sproll L, Stenseth NC (2012) Drought-induced decline in Mediterranean truffle harvest. Nat Clim Chang 2:827–829. https://doi.org/10.1038/nclimate1733
Büntgen U, Oliach D, Martínez-Peña F, Latorre J, Egli S, Krusic PJ (2019) Black truffle winter production depends on Mediterranean summer precipitation. Environ Res Lett 14:74004. https://doi.org/10.1088/1748-9326/ab1880
Callot G (1999) La truffe, la terre, la vie. INRA ed, Versailles
Ceruti A, Fontana A, Nosenzo C (2003) Le specie europee del genere Tuber: una revisione storica. Museo Regionale di Scienze Naturali, Torino
Coleman MD, Bledsoe CS, Lopushinsky W (1989) Pure culture response of ectomycorrhizal fungi to imposed water stress. Can J Bot 67:29–39
Colinas C, Capdevila JM, Oliach D, Fischer CR, Bonet JA (2007) Mapa de aptitud para el cultivo de la trufa negra (Tuber melanosporum Vitt.) en Catalunya, Centre Tecnològic Forestal de Catalunya Ed., Solsona
Cramer W, Guiot J, Fader M, Garrabou J, Gattuso JP, Iglesias A, Lange MA, Lionello P, Llasat MC, Paz S, Peñuelas J, Snoussi M, Toreti A, Tsimplis MN, Xoplaki E (2018) Climate change and interconnected risks to sustainable development in the Mediterranean. Nature Clim Change 8:972–980. https://doi.org/10.1038/s41558-018-0299-2
Datta S, Taghvaeian S, Stivers J (2017) Understanding soil water content and thresholds for irrigation management. Division of Agricultural Science and Natural Resource. Oklahoma Cooperative Extension Service. BAE-1537, pp 1–7.https://doi.org/10.13140/RG.2.2.35535.89765
Díaz-Pérez JC, Dean Batal K (2002) Colored plastic film mulches affect tomato growth and yield via changes in root-zone temperature. J Am Soc Hortic Sci 127:127–135. https://doi.org/10.21273/jashs.127.1.127
Egli S (2011) Mycorrhizal mushroom diversity and productivity – an indicator of forest health? Ann For Sci 68:81–88. https://doi.org/10.1007/s13595-010-0009-3
Fotelli MN, Radoglou KM, Constantinidou HI (2000) Water stress responses of seedlings of four Mediterranean oak species. Tree Physiol 20(16):1065–75. https://doi.org/10.1093/treephys/20.16.1065
Fischer CR, Colinas C (1996) Methodology for the certification of Quercus ilex seedlings inoculated with Tuber melanosporum for commercial application. First International Conference on Mycorrhiza, Berkeley, California.
Garcia-Barreda S, Sánchez S, Marco P, Serrano-Notivoli R (2019) Agro-climatic zoning of Spanish forests naturally producing black truffle. Agric For Meteorol 269–270:231–238. https://doi.org/10.1016/j.agrformet.2019.02.020
Garcia-Barreda S, Camarero J, Vicente-Serrano S, Serrano-Notivoli R (2020) Variability and trends of black truffle production in Spain (1970–2017): linkages to climate, host growth, and human factors. Agric For Meteorol 287:107951. https://doi.org/10.1016/J.AGRFORMET.2020.107951
Giorgi F (2006) Climate change hot-spots. Geophys Res Lett 33:L08707. https://doi.org/10.1029/2006GL025734
Gómez-Molina E, Sánchez S, Parladé J, Cirujeda A, Puig-Pey M, Marco P, García-Barreda S (2020) Glyphosate treatments for weed control affect early stages of root colonization by Tuber melanosporum but not secondary colonization. Mycorrhiza 13:1–9. https://doi.org/10.1007/s00572-020-00990-8
Gordon GG, Foshee WG, Reed ST, Brown JE, Vinson E, Woods FM (2008) Plastic mulches and row covers on growth and production of summer squash. Int J Veg Sci 14:322–338. https://doi.org/10.1080/19315260802215830
Gryndler M, Trilčová J, Hršelová H, Streiblovà E, Gryndlerovà H, Jansa J (2013) Tuber aestivum Vittad. mycelium quantified: advantages and limitations of a qPCR approach. Mycorrhiza 23:341–348. https://doi.org/10.1007/s00572-012-0475-6
Hall IR, Yun W, Amicucci A (2003) Cultivation of edible ectomycorrhizal mushrooms. Trends Biotechnol 21:433–438. https://doi.org/10.1016/S0167-7799(03)00204-X
Jiménez MN, Pinto JR, Ripoll MA, Sánchez-Miranda A, Navarro FB (2017) Impact of straw and rock-fragment mulches on soil moisture and early growth of holm oaks in a semiarid area. CATENA 152:198–206. https://doi.org/10.1016/j.catena.2017.01.021
Kader MA, Singha A, Begum MA, Jewel A, Khan FH, Khan NI (2019) Mulching as water-saving technique in dryland agriculture. Bull Natl Res Cent 43:147. https://doi.org/10.1186/s42269-019-0186-7
Le Tacon F, Delmas J, Gleyze R, Bouchard D (1982). Effect of soil water regime and fertilization on fructification of the black truffle of Perigord (Tuber melanosporum Vitt.) in south east of France. ACTA OECOL. OECOL. APPL: 3(4):291–306.
Le Tacon F, Zeller B, Plain C, Hossann C, Bréchet C, Robin C (2013) Carbon transfer from the host to Tuber melanosporum mycorrhizas and ascocarps followed using a 13C pulse-labeling technique. PLoS One 8(5):e64626. https://doi.org/10.1371/journal.pone.0064626
Le Tacon F, Rubini A, Murat C, Riccioni C, Robin C, Belfiori B, Zeller B, De la Varga H, Akroume E, Deveau A, Martin F (2016). Certainties and uncertainties about the life cycle of the Périgord black truffle (Tuber melanosporum Vittad.). Annals of Forest Science.73(1):105–17. https://doi.org/10.1007/s13595-015-0461-1
Le Tacon F (2017) Les truffes. Ecologie, biologie et domestication. AgroParisTech, Nancy
Mello A, Murat C, Bonfante P (2006) Truffles: much more than a prized and local fungal delicacy. FEMS Microbiol Lett 260:1–8. https://doi.org/10.1111/j.1574-6968.2006.00252.x
Molinier V, Bouffaud M-L, Castel T, Mounier A, Colombet A, Recorbet G, Frochot H, Wipf D (2013) Monitoring the fate of a 30-year-old truffle orchard in Burgundy: from Tuber melanosporum to Tuber aestivum. Agroforest Syst 87:1439–1449. https://doi.org/10.1007/s10457-013-9649-2
Moser B, Büntgen U, Molinier V, Peter M, Sproll L, Stobbe U, Tegel W, Egli S (2017) Ecological indicators of Tuber aestivum habitats in temperate European beech forests. Fungal Ecol 29:59–66. https://doi.org/10.1016/j.funeco.2017.06.002
Murat C (2015) Forty years of inoculating seedlings with truffle fungi: past and future perspectives. Mycorrhiza 25:77–81. https://doi.org/10.1007/s00572-014-0593-4
Oliach D, Colinas C, Castaño C, Fisher CR, Bolaño F, Bonet JA, Oliva J (2020a) The influence of forest surroundings on the soil fungal community of black truffle (Tuber melanosporum) plantations. Forest Ecol Manag 470–471:118212. https://doi.org/10.1016/j.foreco.2020.118199
Oliach D, Morte A, Sánchez S, Navarro-Ródenas A, Marco P, Gutiérrez A, Martín-Santafé M, Fischer C, Albisu LM, García-Barreda S, Martínez-Peña F, Colinas C (2020b) Las trufas y las turmas. In: Sánchez-González M, Calama R, Bonet JA (eds) Los productos forestales no madereros en España: Del monte a la industria. Monografías INIA: Serie Forestal, 31, Ministerio de Ciencia e Innovación, Gobierno de España, Madrid
Olivier JM (2000) Progress in the cultivation of truffles. In: van Griensven LJL (ed) Proceedings of the 15th international congress on the science and cultivation of edible fungi, Maastricht, Netherlands, 15–19 May, 2000. AA Balkema, Rotterdam, pp 937–942
Olivera A, Fischer CR, Bonet JA, Martínez de Aragón J, Oliach D, Colinas C (2011) Weed management and irrigation are key treatments in emerging black truffle (Tuber melanosporum) cultivation. New For 42:227–239. https://doi.org/10.1007/s11056-011-9249-9
Olivera A, Bonet JA, Oliach D, Colinas C (2014a) Time and dose of irrigation impact Tuber melanosporum ectomycorrhiza proliferation and growth of Quercus ilex seedling hosts in young black truffle orchards. Mycorrhiza 24:73–78. https://doi.org/10.1007/s00572-013-0545-4
Olivera A, Bonet JA, Palacio L, Liu B, Colinas C (2014b) Weed control modifies Tuber melanosporum mycelial expansion in young oak plantations. Ann For Sci 71:495–504. https://doi.org/10.1007/s13595-014-0360-x
Ori F, Leonardi P, Stagnini E, Balestrini V, Iotti M, Zambonelli A (2018) Is Tuber brumale a threat to T. melanosporum and T. aestivum plantations? IForest 11:775–780. https://doi.org/10.3832/ifor2785-011
Parladé J, De la Varga H, De Miguel AM, Sáez R, Pera J (2013) Quantification of extraradical mycelium of Tuber melanosporum in soils from truffle orchards in northern Spain. Mycorrhiza 23:99–106. https://doi.org/10.1007/s00572-012-0454-y
Pinheiro JC, Bates DM (2000) Mixed-effects models in S and S-PLUS. Springer, NewYork
Pinheiro JC, Bates DM, DebRoy S, Sakar D (2012) The Nlme Package: linear and nonlinear mixed effects models, R Version 3.
Piñuela Y, Alday JG, Oliach D, Bolaño F, Colinas C, Bonet JA (2020) Use of inoculator bacteria to promote Tuber melanosporum root colonization and growth on Quercus faginea saplings. Forests 11:792. https://doi.org/10.3390/f11080792
Qin W, Hu C, Oenema O (2015) Soil mulching significantly enhances yields and water and nitrogen use efficiencies of maize and wheat: a meta-analysis. Sci Rep 5:1–13. https://doi.org/10.1038/srep16210
Queralt M, Parladé J, Pera J, De Miguel AM (2017) Seasonal dynamics of extraradical mycelium and mycorrhizas in a black truffle (Tuber melanosporum) plantation. Mycorrhiza 27:565–576. https://doi.org/10.1007/s00572-017-0780-1
R Core Team. 2017. R: A language and environment for statistical computing, version 3.5.3. Vienna, Austria: R Foundation for Statistical Computing.
Reyna S, García-Barreda S (2014) Black truffle cultivation: a global reality. For Syst 23:317–328. https://doi.org/10.5424/fs/2014232-04771
Ricard JM, Bergounoux F, Callot G, Chevalier G, Olivier JM, Pargney JC, Sourzat P (2003) La truffe. Guide technique de trufficulture, Centre Technique Interprofessionnel des Fruits et Legumes CTIFL, Paris
Sánchez S, De Miguel AM and Sáez, R, Martín-Santafé M, Águeda B, Barriuso J, García-Barreda S, Salvador-Alcalde D, Reyna S (2016) Summer truffle in the Iberian Peninsula: current status and crop potential. ITEA Informacion Tecnica Economica Agraria 112(1):20–33. https://doi.org/10.12706/itea.2016.007
Smith SE, Read DJ (1997) Mycorrhizal symbiosis. Academic Press, London
Stobbe U, Büntgen U, Sproll L, Tegel W, Egli S, Fink S (2012) Spatial distribution and ecological variation of re-discovered German truffle habitats. Fungal Ecol 5:591–599. https://doi.org/10.1016/j.funeco.2012.02.001
Stobbe U, Egli S, Tegel W, Peter M (2013) Potential and limitations of Burgundy truffle cultivation. Appl Microbiol Biotechnol 97:5215–5224. https://doi.org/10.1007/s00253-013-4956-0
Suz LM, Martín MP, Oliach D, Fisher CR, Colinas C (2008) Mycelial abundance and other factors related to truffle productivity in Tuber melanosporum-Quercus ilex orchards. FEMS Microbiol Lett 285:72–78. https://doi.org/10.1111/j.1574-6968.2008.01213.x
Todesco F, Belmondo S, Guignet Y, Laurent L, Fizzala S, Le Tacon F, Murat C (2019) Soil temperature and hydric potential influences the monthly variations of soil Tuber aestivum DNA in a highly productive orchard. Sci Rep 9:1–10. https://doi.org/10.1038/s41598-019-49602-2
Vicente-Serrano SM, López-Moreno JI, Beguería S, Lorenzo-Lacruz J, Sánchez-Lorenzo A, García-Ruiz JM, Azorín-Molina C, Morán-Tejeda E, Revuelto J, Trigo R, Coelho F, Espejo F (2014) Evidence of increasing drought severity caused by temperature rise in southern Europe. Environ Res Lett 9:044001. https://doi.org/10.1088/1748-9326/9/4/044001
Watson RJ, Blackwell B (2000) Purification and characterization of a common soil component which inhibit the polymerase chain reaction. Can J Microbiol 46:633–642. https://doi.org/10.1139/w00-043
Zambonelli A, Iotti M, Zinoni F, Dallavalle E, Hall IR (2005) Effect of mulching on Tuber uncinatum ectomycorrhizas in an experimental truffière. N Z J Crop Hortic Sci 33:65–73. https://doi.org/10.1080/01140671.2005.9514332
Zampieri E, Murat C, Cagnasso M, Bonfante P, Mello A (2010) Soil analysis reveals the presence of an extended mycelial network in a Tuber magnatum truffle-ground. FEMS Microbiol Ecol 71:43–49. https://doi.org/10.1111/j.1574-6941.2009.00783.x
Acknowledgments
We would like to thank Mr. Didac Espasa (Vice President of Catalonian Truffle growers’ association, PROTOCAT and owner of the company Tofona de la Conca) and Dr. Simon Egli for their valuable contribution. We are grateful to Ms. Caroline Woods for the linguistic revision of the text. Y.P. thanks the University of Lleida for her contract (UdL-Impuls).
Funding
This work was supported by the Project INNOVATRUF (PECT El bosc, el primer recurs de l’economia verda—Fons Europeu de Desenvolupament Regional de la Unió Europea-Programa operatiu FEDER de Catalunya 2014–2020), by the Spanish Ministry of Science, Innovation and Universities, grant RTI2018-099315-A-I00, by the ‘Direcció General d’Ecosistemes Forestals i Gestió del Medi Departament d’Agricultura, Ramaderia, Pesca i Alimentació’ of ‘Generalitat de Catalunya’ and by the BLACKDYNAMITE project, funded by the WSL and CTFC. J.G.A. was supported by the Ramon y Cajal fellowship (RYC-2016-20528), D.O. received support from the ‘Secretaria d’Universitats i Recerca del Departament d’Economia i Coneixement de la Generalitat de Catalunya’ through the program of ‘Doctorats Industrials’; F.B.’s salary was partially funded by the Ministry of Science, Innovation, and Universities through the National Agency of Research (PTA2017-14041-I), and J.A.B. benefitted from a Serra-Húnter Fellowship provided by the Generalitat of Catalunya.
Author information
Authors and Affiliations
Contributions
All authors contributed to the study conception and design. YP, DO and FB performed the experiments. YP performed laboratory analyses under the supervision of CCa and JAB. YP and JGA analysed the data. YP wrote the manuscript with inputs from JAB, JGA, FB, DO, CCa and CCo. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Conflicts of Interest
The authors declare that they have no conflict of interest.
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Piñuela, Y., Alday, J.G., Oliach, D. et al. White mulch and irrigation increase black truffle soil mycelium when competing with summer truffle in young truffle orchards. Mycorrhiza 31, 371–382 (2021). https://doi.org/10.1007/s00572-020-01018-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00572-020-01018-x