Tuber wenchuanense, a holarctic truffle with a wide range of host plants and description of its ectomycorrhiza with spruce

Mycorrhiza - Tập 33 Số 1 - Trang 45-58 - 2023
Mleczko, Piotr1, Hilszczańska, Dorota2, Karpowicz, Filip1, Kozak, Maciej3, Leonardi, Marco4, Rosa-Gruszecka, Aleksandra2, Tereba, Anna2, Pacioni, Giovanni4
1Institute of Botany, Faculty of Biology, Jagiellonian University, Kraków, Poland
2Department of Forest Ecology, Forest Research Institute, Sękocin Stary, Raszyn, Poland
3Kraków, Poland
4Department of Life, Health, and Environmental Sciences, University of l'Aquila, l'Aquila, Italy

Tóm tắt

Tuber wenchuanense ascomata (Ascomycota, Pezizales), a species originally described from Sichuan (China), were found in the Tatra Mountains in southern Poland. The purpose of this work was to (i) report and assess the first case of the holarctic natural distribution of a Tuber species, (ii) amend the original description of the species, (iii) summarize data on its host plants and (iv) describe its ectomycorrhiza. Specimens of Tuber wenchuanense from the Tatra Mountains were studied morphologically and molecularly. The ectomycorrhiza of this truffle with Picea abies was described for the first time. The distribution of T. wenchuanense, which is reconstructed based on sequences deposited in the publicly available nucleotide sequence databases, makes it the first holarctic Tuber species and the one with the northernmost habitat. In fact, its habitat is confined mainly to mountain coniferous forests and alpine and arctic tundra; although, according to known observations, the fruiting bodies of T. wenchuanense can be produced only under conifers. Based on the sequences of the internal transcribed spacer, this species appears to have low genetic variability over the entire distribution range. The phylogenetic tree showed that some of the unidentified phylotypes from the Rufum clade found by other researchers belong to T. wenchuanense. The ecological implications of these findings are discussed.

Tài liệu tham khảo

citation_journal_title=Mycol Progr; citation_title=Fungal relationships and structural identity of their ectomycorrhizae; citation_author=R Agerer; citation_volume=5; citation_issue=2; citation_publication_date=2006; citation_pages=67-107; citation_doi=10.1007/s11557-006-0505-x; citation_id=CR1 Agerer R, Rambold G (2004–2013) [first posted on 2004–06–01; most recent update: 2011–01–10]. DEEMY—an information system for characterization and determination of ectomycorrhizae. www.deemy.de – München, Germany Agerer R (1991) Characterization of ectomycorrhiza. In: Norris JR, Read DJ, Varma AK (eds) Techniques for the study of mycorrhiza. Methods Microbiol 23:25–73 citation_journal_title=Scand J for Res; citation_title=Radial stem growth of Picea abies in relation to spatial variation in soil moisture conditions; citation_author=G Alavi; citation_volume=11; citation_issue=1–4; citation_publication_date=1996; citation_pages=209-219; citation_doi=10.1080/02827589609382930; citation_id=CR4 citation_journal_title=J Mol Biol; citation_title=Basic local alignment search tool; citation_author=SF Altschul, W Gish, W Miller, EW Myers, DJ Lipman; citation_volume=215; citation_issue=3; citation_publication_date=1990; citation_pages=403-410; citation_doi=10.1016/S0022-2836(05)80360-2; citation_id=CR5 citation_journal_title=New Phytol; citation_title=Habitat specialisation controls ectomycorrhizal fungi above the treeline in the European Alps; citation_author=R Arraiano-Castilho, MI Bidartondo, T Niskanen, JJ Clarkson, I Brunner, S Zimmermann, B Senn-Irlet, B Frey, U Peintner, T Mrak, LM Suz; citation_volume=229; citation_issue=5; citation_publication_date=2021; citation_pages=2901-2916; citation_doi=10.1111/nph.17033; citation_id=CR6 citation_journal_title=Conserv Genet; citation_title=History, genetic differentiation and conservation strategies for disjunct populations of Sibiraea species from Southeastern Europe and Asia; citation_author=D Ballian, T Grebenc, G Božič, V Melnik, T Wraber, H Kraigher; citation_volume=7; citation_publication_date=2006; citation_pages=895-907; citation_doi=10.1007/s10592-006-9131-z; citation_id=CR7 citation_journal_title=Mol Ecol; citation_title=A global meta-analysis of Tuber ITS rDNA sequences: species diversity, host associations and long-distance dispersal; citation_author=GM Bonito, AP Gryganskyi, JM Trappe, R Vilgalys; citation_volume=19; citation_publication_date=2010; citation_pages=4994-5008; citation_doi=10.1111/j.1365-294X.2010.04855.x; citation_id=CR8 citation_journal_title=PLoS ONE; citation_title=Historical biogeography and diversification of truffles in the Tuberaceae and their newly identified southern hemisphere sister lineage; citation_author=G Bonito, ME Smith, M Nowak, RA Healy, G Guevara, E Cázares, A Kinoshita, ER Nouhra, LS Domínguez, L Tedersoo, C Murat, Y Wang, BA Moreno, DH Pfister, K Nara, A Zambonelli, JM Trappe, R Vilgalys; citation_volume=8; citation_issue=1; citation_publication_date=2013; citation_doi=10.1371/journal.pone.0052765; citation_id=CR9 Bonito GM, Smith ME (2016) General systematic position of the truffles: evolutionary theory. Chap.1 In Zambonelli A,Iotti M, Murat C (eds) True Truffle (Tuber spp.) in the world. Soil Biology 47. Springer International Publishing, Cham, Switzerland. pp.3–18 citation_journal_title=Mycol Prog; citation_title=Molecular and morphological identification of truffle-producing Tuber species in New Zealand; citation_author=SR Bulman, SB Visnovsky, IR Hall, A Guerin-Laguette, Y Wang; citation_volume=9; citation_publication_date=2010; citation_pages=205-214; citation_doi=10.1007/s11557-009-0626-0; citation_id=CR12 citation_title= in Europe: distribution, habitat, usage and threats; citation_inbook_title=European Atlas of Forest Tree Species; citation_publication_date=2016; citation_pages=114-116; citation_id=CR13; citation_author=G Caudullo; citation_author=W Tinner; citation_author=D Rigo; citation_publisher=Publication Office of the European Union citation_journal_title=PLoS ONE; citation_title=Species recognition and cryptic species in the Tuber indicum Complex; citation_author=J Chen, S-X Guo, P-G Liu; citation_volume=6; citation_issue=1; citation_publication_date=2011; citation_doi=10.1371/journal.pone.0014625; citation_id=CR14 Crous PW, Cowan DA, Maggs-Kölling G, Yilmaz N, Thangavel R, Wingfield MJ, Noordeloos ME, Dima B, Brandrud TE, Jansen GM et al. (2021) Fungal Planet description sheets: 1182–1283. Pers: Mol Phylogeny Evol Fungi 46:313–528 citation_journal_title=Mycotaxon; citation_title=Tuber subsphaerospermum and Tuber wenchuanense - two new species with spino-reticulate ascospores; citation_author=L Fan, JZ Cao, CL Hou; citation_volume=123; citation_publication_date=2013; citation_pages=95-101; citation_doi=10.5248/123.95; citation_id=CR16 Fineschi S, Cozzolino S, Migliaccio M, Vendramin GG (2004) Genetic variation of relic tree species: the case of Mediterranean Zelkova abelicea (Lam.) Boisser and Z. sicula Di Pasquale, Garfı̀ and Quézel (Ulmaceae). For Ecol Manag 197(1–3):273–278 citation_journal_title=Mol Ecol; citation_title=ITS primers with enhanced specificity for basidiomycetes application to the identification of mycorrhizae and rusts; citation_author=M Gardes, TD Bruns; citation_volume=2; citation_publication_date=1993; citation_pages=113-118; citation_doi=10.1111/j.1365-294X.1993.tb00005.x; citation_id=CR18 citation_journal_title=Mycologia; citation_title=Tuber brennemanii and Tuber floridanum: Two new Tuber species are among the most commonly detected ectomycorrhizal taxa within commercial pecan (Carya illinoinensis) orchards; citation_author=AC Grupe, MA Sulzbacher, T Grebenc, R Healy, G Bonito, ME Smith; citation_volume=110; citation_publication_date=2018; citation_pages=780-790; citation_doi=10.1080/00275514.2018.1490121; citation_id=CR19 citation_journal_title=Nucleic Acids Symp Ser; citation_title=BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/ 98/NT; citation_author=TA Hall; citation_volume=41; citation_publication_date=1999; citation_pages=95-98; citation_id=CR20 citation_journal_title=Can J Bot; citation_title=Characterization of Dryas octopetala ectomycorrhizas from limestone karst vegetation, western Ireland; citation_author=TJ Harrington, DT Mitchell; citation_volume=80; citation_issue=9; citation_publication_date=2002; citation_pages=970-982; citation_doi=10.1139/b02-082; citation_id=CR21 Healy RA, Bonito GM, Smith ME (2016) A brief overview of systematics, taxonomy and ecology of the Tuber rufum clade. Chap.8, In Zambonelli A, Iotti M, Murat C (eds) True truffle (Tuber spp.) in the world Soil. Biology 47, Springer International Publishing, Cham, Switzerland. pp 125–136 citation_journal_title=FEMS Microbiol Lett; citation_title=Selection of a set of specific primers for the identification of Tuber rufum: a truffle species with high genetic variability; citation_author=M Iotti, A Amicucci, G Bonito, E Bonuso, V Stocchi, A Zambonelli; citation_volume=277; citation_issue=2; citation_publication_date=2007; citation_pages=223-231; citation_doi=10.1111/j.1574-6968.2007.00963.x; citation_id=CR23 citation_journal_title=Mol Biol Evol; citation_title=MAFFT multiple sequence alignment software version 7: improvements in performance and usability; citation_author=K Katoh, DM Standley; citation_volume=30; citation_publication_date=2013; citation_pages=772-780; citation_doi=10.1093/molbev/mst010; citation_id=CR24 citation_journal_title=J Mol Evol; citation_title=A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences; citation_author=M Kimura; citation_volume=16; citation_publication_date=1980; citation_pages=111-120; citation_doi=10.1007/BF01731581; citation_id=CR25 citation_journal_title=Mycorrhiza; citation_title=Ectomycorrhizae formed by three Japanese truffle species (Tuber japonicum, T. longispinosum, and T. himalayense) on indigenous oak and pine species; citation_author=A Kinoshita, O Keisuke, Y Takashi; citation_volume=28; citation_publication_date=2018; citation_pages=679-690; citation_doi=10.1007/s00572-018-0860-x; citation_id=CR26 citation_title=Ainsworth & Bisby’s Dictionary of the Fungi; citation_publication_date=2008; citation_id=CR27; citation_author=P Kirk; citation_author=PF Cannon; citation_author=DW Minter; citation_author=JA Stalpers; citation_publisher=CAB International citation_journal_title=Microorganisms; citation_title=The taxon hypothesis paradigm—on the unambiguous detection and communication of taxa; citation_author=U Kõljalg, HR Nilsson, D Schigel, L Tedersoo, KH Larsson, TW May, AFS Taylor, T Stjernegaard Jeppesen, T Guldberg Frøslev, BD Lindahl, K Põldmaa, I Saar, A Suija, A Savchenko, I Yatsiuk, K Adojaan, F Ivanov, T Piirmann, R Pöhönen, A Zirk, K Abarenkov; citation_volume=8; citation_issue=12; citation_publication_date=2020; citation_pages=1910; citation_doi=10.3390/microorganisms8121910; citation_id=CR28 citation_journal_title=Mol Biol Evol; citation_title=MEGA X: Molecular Evolutionary Genetics Analysis across computing platforms; citation_author=S Kumar, G Stecher, M Li, C Knyaz, K Tamura; citation_volume=35; citation_publication_date=2018; citation_pages=1547-1549; citation_doi=10.1093/molbev/msy096; citation_id=CR29 citation_journal_title=Bioinformatics; citation_title=AliView: a fast and lightweight alignment viewer and editor for large datasets; citation_author=A Larsson; citation_volume=30; citation_issue=22; citation_publication_date=2014; citation_pages=3276-3278; citation_doi=10.1093/bioinformatics/btu531; citation_id=CR30 citation_journal_title=Mycorrhiza; citation_title=Climatic variations explain annual fluctuations in French Périgord black truffle whole sale markets but do not explain the decrease in black truffle production over the last 48 years; citation_author=F Tacon, B Marçais, M Courvoisier, C Murat, P Montpied, M Becker; citation_volume=24; citation_publication_date=2014; citation_pages=115-125; citation_doi=10.1007/s00572-014-0568-5; citation_id=CR31 citation_journal_title=Mycologia; citation_title=Two new species of Tuber previously reported as Tuber malacodermum; citation_author=M Leonardi, A Paz-Conde, G Guevara, D Salvi, G Pacioni; citation_volume=111; citation_publication_date=2019; citation_pages=676-689; citation_doi=10.1080/00275514.2019.1603777; citation_id=CR32 Leonardi M, Iotti M, Mello A, Vizzini A, Paz-Conde A, Trappe J, Pacioni G (2021a) Typification of the four most investigated and valuable truffles: Tuber aestivum Vittad., T. borchii Vittad., T. magnatum Picco and T. melanosporum Vittad. Cryptogam Mycol 41(10):1–22 Leonardi M, Iotti M, Pacioni G, Hall I, Zambonelli A (2021b) Truffles: biodiversity, ecological significances and biotechnological applications. In Abdel-Azeem A.M., Yadav A.N. Yadav, Usmani Z. (eds) Industrially Important Fungi for Sustainable Development. Vol. 1: Biodiversity and Ecological Perspectives. Springer Nature. pp.107–146 citation_journal_title=Mol Phylogenet Evol; citation_title=Phylogeny and intraspecific variability of holoparasitic Orobanche (Orobanchaceae) inferred from plastid rbcL sequences; citation_author=J-F Manen, C Habashi, D Jeanmonod, J-M Park, GM Schneeweiss; citation_volume=33; citation_publication_date=2004; citation_pages=482-500; citation_doi=10.1016/j.ympev.2004.06.010; citation_id=CR35 citation_title=Molecular evolution and phylogenetics; citation_publication_date=2000; citation_id=CR36; citation_author=M Nei; citation_author=S Kumar; citation_publisher=Oxford University Press citation_journal_title=Mycorrhiza; citation_title=Crested porcupines (Hystrix cristata): mycophagist spore dispersers of the ectomycorrhizal truffle Tuber aestivum; citation_author=F Ori, J Trappe, M Leonardi, M Iotti, G Pacioni; citation_volume=28; citation_issue=5; citation_publication_date=2018; citation_pages=561-565; citation_doi=10.1007/s00572-018-0840-1; citation_id=CR37 citation_journal_title=Fungal Biol; citation_title=Effect of slug mycophagy on Tuber aestivum spores; citation_author=F Ori, M Menotta, M Leonardi, M Amicucci, A Zambonelli, H Covès, M-A Selosse, L Schneider-Maunoury, G Pacioni, M Iotti; citation_volume=125; citation_publication_date=2021; citation_pages=796-805; citation_doi=10.1016/j.funbio.2021.05.002; citation_id=CR38 citation_journal_title=Mycorrhiza; citation_title=Instrumental monitoring of the birth and development of truffles in a Tuber melanosporum orchard; citation_author=G Pacioni, M Leonardi, P Carlo, D Ranalli, A Zinni, G Laurentiis; citation_volume=24; citation_publication_date=2014; citation_pages=65-72; citation_doi=10.1007/s00572-014-0561-z; citation_id=CR39 Pacioni G, Comandini O (1999) Tuber. In: Cairney JWG, Chambers SM (eds) Ectomycorrhizal fungi. Key Genera in Profile. Springer, Berlin, Heidelberg, pp 163–186 citation_journal_title=Nova Hedw; citation_title=Ektomykorrhizen von Tuber melanosporum, Tuber mesentericum und Tuber rufum (Tuberales) an Corylus avellana; citation_author=T Rauscher, R Agerer, G Chevalier; citation_volume=61; citation_publication_date=1995; citation_pages=281-322; citation_id=CR41 Rauscher T, Chevalier G (1995) Tuber rufum. In Agerer R (ed) Colour Atlas of Ectomycorrhizae, plate 89, Einhorn-Verlag, Schwäbisch Gmünd Rayner RW (1970) A Mycological colour chart. Commonwealth Mycological Institute: Kew, U.K citation_journal_title=Proc Natl Acad Sci USA; citation_title=DNA sequencing with chain-terminating inhibitors; citation_author=F Sanger, S Nicklen, AR Coulson; citation_volume=74; citation_publication_date=1977; citation_pages=5463-5467; citation_doi=10.1073/pnas.74.12.5463; citation_id=CR44 citation_journal_title=Nucleic Acids Res; citation_title=GenBank; citation_author=EW Sayers, M Cavanaugh, K Clark, KD Pruitt, CL Schoch, ST Sherry, I Karsch-Mizrachi; citation_volume=49; citation_issue=D1; citation_publication_date=2021; citation_pages=D92-D96; citation_doi=10.1093/nar/gkaa1023; citation_id=CR45 citation_journal_title=J Ecol; citation_title=Exploiting mycorrhizas in broad daylight: partial mycoheterotrophy is a common nutritional strategy in meadow orchids; citation_author=JMI Schiebold, MI Bidartondo, F Lenhard, A Makiola, G Gebauer; citation_volume=106; citation_publication_date=2018; citation_pages=168-178; citation_doi=10.1111/1365-2745.12831; citation_id=CR46 citation_journal_title=New Phytol; citation_title=Two ectomycorrhizal truffles, Tuber melanosporum and T. aestivum, endophytically colonise roots of non-ectomycorrhizal plants in natural environments; citation_author=L Schneider-Maunoury, A Deveau, M Moreno, F Todesco, S Belmondo, C Murat, P-E Courty, M Jąkalski, M-A Selosse; citation_volume=225; citation_publication_date=2020; citation_pages=2542-2556; citation_doi=10.1111/nph.16321; citation_id=CR47 citation_journal_title=Microb Ecol; citation_title=Chlorophyllous and achlorophyllous specimens of Epipactis microphylla (Neottieae, Orchidaceae) are associated with ectomycorrhizal septomycetes, including truffles; citation_author=MA Selosse, G Scappaticci, A Faccio, P Bonfante; citation_volume=47; citation_publication_date=2004; citation_pages=416-426; citation_doi=10.1007/s00248-003-2034-3; citation_id=CR48 Shengxian Z (1995) Ecological and geographical distribution of Larix and cultivation of its major species in Southwestern China. In: Ecology and Management of Larix Forests: A Look Ahead: Proceedings of an International Symposium, Whitefish, Montana, USA October 5–9, 1992 (No. 319, p. 38). US Department of Agriculture, Forest Service, Intermountain Research Station citation_journal_title=Appl Microbiol Biotechnol; citation_title=Potential and limitations of Burgundy truffle cultivation; citation_author=U Stobbe, S Egli, W Tegel, M Peter, L Sproll, U Büntgen; citation_volume=97; citation_issue=12; citation_publication_date=2013; citation_pages=5215-5224; citation_doi=10.1007/s00253-013-4956-0; citation_id=CR50 citation_journal_title=Mycotaxon; citation_title=Tuber magnatum in Thailand, a first report from Asia; citation_author=N Suwannarach, J Kumla, J Meerak, J Lumvong; citation_volume=132; citation_issue=3; citation_publication_date=2017; citation_pages=635-642; citation_doi=10.5248/132.635; citation_id=CR51 citation_journal_title=Plant Mol Biol; citation_title=Universal primers for amplification of three non-coding regions of chloroplast DNA; citation_author=P Taberlet, L Gielly, G Pautou, J Bouvet; citation_volume=17; citation_publication_date=1991; citation_pages=1105-1109; citation_doi=10.1007/BF00037152; citation_id=CR52 citation_journal_title=Plant Soil; citation_title=Insight into the truffle brûlé: tripartite interactions between the black truffle (Tuber melanosporum), holm oak (Quercus ilex) and arbuscular mycorrhizal plants; citation_author=E Taschen, VB Sauve, J Parladé, D Tuinen, Y Aumeeruddy-Thomas, B Assenat, M-A Selosse, F Richard; citation_volume=446; citation_publication_date=2020; citation_pages=577-594; citation_doi=10.1007/s11104-019-04340-2; citation_id=CR53 citation_journal_title=Ecol Monogr; citation_title=A first comprehensive census of fungi in soil reveals both hyperdiversity and fine-scale niche partitioning; citation_author=DL Taylor, TN Hollingsworth, JW McFarland, NJ Lennon, C Nusbaum, RW Ruess; citation_volume=84; citation_issue=1; citation_publication_date=2014; citation_pages=3-20; citation_doi=10.1890/12-1693.1; citation_id=CR54 citation_journal_title=Science; citation_title=Global diversity and geography of soil fungi; citation_author=L Tedersoo, M Bahram, S Polme, U Koljalg, NS Yorou, R Wijesundera, LV Ruiz, AM Vasco-Palacios, PQ Thu, A Suija, ME Smith, C Sharp, E Saluveer, A Saitta, M Rosas, T Riit, D Ratkowsky, K Pritsch, K Põldmaa, M Piepenbring, C Phosri, M Peterson, K Parts, K Pärtel, E Otsing, E Nouhra, AL Njouonkou, RH Nilsson, LN Morgado, J Mayor, TW May, L Majuakim, DJ Lodge, SS Lee, L-H Kohout, null P, Hosaka K, Hiiesalu I, Henkel TW, Harend H, Guo L-D, Greslebin A, Grelet G, Geml J, Gates G, Dunstan W, Dunk C, Drenkhan R, Dearnaley J, De Kesel A, Dang RT, Chen X, Buegger F, Brearley FQ, Bonito G, Anslan S, Abell S, Abarenkov K, ; citation_volume=346; citation_issue=6213; citation_publication_date=2014; citation_pages=1256688-1256688; citation_doi=10.1126/science.1256688; citation_id=CR55 citation_journal_title=Ecosphere; citation_title=Distribution and drivers of ectomycorrhizal fungal communities across the North American Arctic; citation_author=I Timling, A Dahlberg, DA Walker, M Gardes, JY Charcosset, JM Welker, DL Taylor; citation_volume=3; citation_issue=11; citation_publication_date=2012; citation_pages=111; citation_doi=10.1890/ES12-00217.1; citation_id=CR56 Trappe JM, Molina R, Luoma DL, Cázares E, Pilz D, Smith JE, Castellano MA, Miller SL, Trappe MJ (2009) Diversity, ecology and conservation of truffle fungi in forests of the Pacific Northwest; Gen. Tech. Rep. PNW-GTR-772; USDA Forest Service, Pacific Northwest Research Station: Portland, OR, USA Urban A (2016) Truffles and small mammals. Cuap.21. In: Zambonelli A, Iotti M, Murat C (eds) True Truffle (Tuber spp.) in the World. Soil Biology 47, Springer International Publishing, Cham, Switzerland, pp.353–374 citation_journal_title=New Phytol; citation_title=Global patterns of ectomycorrhizal introductions; citation_author=EC Vellinga, BE Wolfe, A Pringle; citation_volume=181; citation_publication_date=2009; citation_pages=960-973; citation_doi=10.1111/j.1469-8137.2008.02728.x; citation_id=CR59 citation_journal_title=Silvics of North America; citation_title=Picea mariana (Mill.) BSP, black spruce; citation_author=LA Viereck, WF Johnston, RM Burns, BH Honkala; citation_volume=1; citation_publication_date=1990; citation_pages=227-237; citation_id=CR60 Wan S-P, Yu F-Q, Tang L, Wang R, Wang Y, Liu P-G, Wang X-H, Zheng Y (2016). Ectomycorrhizae of Tuber huidongense and T. liyuanum with Castanea mollissima and Pinus armandii. Mycorrhiza 26(3):249–256 citation_journal_title=Fungal Ecol; citation_title=Morphological, mycorrhizal and molecular characterization of Finnish truffles belonging to the Tuber anniae species-complex; citation_author=X-H Wang, GMN Benucci, X-D Xie, G Bonito, M Leisola, P-G Liu, S Shamekh; citation_volume=6; citation_publication_date=2013; citation_pages=269-280; citation_doi=10.1016/j.funeco.2013.03.002; citation_id=CR62 citation_journal_title=PCR Protocols: a Guide to Methods and Applications; citation_title=Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics; citation_author=TJ White, T Bruns, SJWT Lee, J Taylor; citation_volume=18; citation_publication_date=1990; citation_pages=315-322; citation_id=CR63 citation_title=Mycophagy and spore dispersal by vertebrates; citation_inbook_title=The fungal community: its organization and role in the ecosystem; citation_publication_date=2017; citation_pages=347-358; citation_id=CR64; citation_author=A Zambonelli; citation_author=F Ori; citation_author=I Hall; citation_publisher=CRC