Abstract
Truffles, as hypogeous, ectomycorrhizal fungi, have no means to actively discharge spores into the environment and thus depend on mycophagists for spore dispersal. After consumption of fruiting bodies by animals and passage through the digestive tract, the spores are released in faecal pellets. Recently, in the Abruzzo region (Italy), Hystrix cristata has been spotted inside private truffières, but its role in spore dispersal has never been investigated. Here, we report our research on the occurrence of Tuber aestivum spores in porcupine’s faecal contents in a truffière in L’Aquila, Italy, where a H. cristata specimen was photographed. The spores were isolated from faeces by using a suspension of 0.7 M ZnSO4. We also verified degradation and disfiguration of the digested spores’ reticular ornamentation compared to that of fresh spores from ascomata collected inside the truffière, through measurements performed by scanning electron microscopy. A few truffle spores had germinated within the faeces.
References
Amori G, Contoli L, Nappi A (2008) Fauna d'Italia Vol. XLIV. Mammalia II: Erinaceomorpha, Soricomorpha, Lagomorpha, Rodentia. In: Edagricole, Calderini (ed) Il Sole 24 Ore, Bologna, pp 694–706
Ashkannejhad S, Horton TR (2006) Ectomycorrhizal ecology under primary succession on the coastal sand dunes: interactions involving Pinus contorta, suilloid fungi and deer. New Phytol 169:345–354
Bonito GM, Gryganskyi AP, Trappe JM, Vilgalys R (2010) A global meta-analysis of Tuber ITS rDNA sequences: species diversity, host associations and long-distance dispersal. Mol Ecol 19:4994–5008
Bonito G, Smith ME, Nowak M, Healy RA, Guevara G, Cázares E, Kinoshita A, Nouhra ER, Domínguez LS, Tedersoo L, Murat C, Wang Y, Moreno BA, Pfister DH, Nara K, Zambonelli A, Trappe JM, Vilgalys R (2013) Historical biogeography and diversification of truffles in the Tuberaceae and their newly identified southern hemisphere sister lineage. PLoS One 8(1):e52765
Bruno E, Riccardi C (1995) The diet of the crested porcupine Hystrix cristata L., 1758 in a Mediterranean rural area. Z Saugetierkd 60:226–236
Cazares E, Luoma DL, Amaranthus MP, Chambers CL, Lehmkuhl JF (1999) Interaction of fungal sporocarp production with small mammal abundance and diet in Douglas-fir stands of the southern Cascade range. Northwest Sci 73, (Special Issue): 67–76
Claridge AW, Trappe JM (2005) Sporocarp mycophagy: nutritional, behavioral, evolutionary, and physiological aspects. In: Dighton J, White JF, Oudemans P (eds) The fungal community its organization and role in the ecosystem, 3rd edn. CRC Press, Boca Raton, pp 599–611
Colgan W, Claridge W (2002) Mycorrhizal effectiveness of Rhizopogon spores recovered from faecal pellets of small forest-dwelling mammals. Mycol Res 106:314–320
Currah RS, Smreciu EA, Lehesvirta T et al (2000) Fungi in the winter diets of northern flying squirrels and red squirrels in the boreal mixedwood forest of northeastern Alberta. Can J Bot 78:1514–1520
Febbo D, Pellegrini M (1994) Assessorato al Turismo, Regione Abruzzo, CARSA 1994, in collaboration with Legambiente and WWF. Guida alla Fauna, Abruzzo, pp 91–94
Gryndler M, Hršelová H, Soukupová L, Streiblová E, Valda S, Borovička J, Gryndlerová H, Gažo J, Miko M (2011) Detection of summer truffle (Tuber aestivum Vittad.) in ectomycorrhizae and in soil using specific primers. FEMS Microbiol Lett 318:84–89
Hall I, Brown G, Zambonelli A (2007) Taming the truffle. The history, lore, and science of the ultimate mushroom. Timber Press, Portland
Mannina L, Cristinzio M, Sobolev AP, Ragni P, Segre A (2004) High-field nuclear magnetic resonance (NMR) study of truffles (Tuber aestivum Vittadini). J Agric Food Chem 52(26):7988–7996
Maser C, Trappe JM, Nussbaum RA (1978) Fungal-small mammal relationships with emphasis on Oregon coniferous forests. Ecology 59:799–809
Maser C, Claridge AW, Trappe JM (2008) Trees, truffle, and beasts: how forests function. Rutgers University Press, New Brunswick
Mohamed WF (2011) The crested porcupine Hystrix cristata (Linnaeus, 1758) in Misurata, Libya. Eur J Biol Sci 3:9–12
Morini P (2011) Presenza dell’istrice (Hystrix cristata) nel Parco Regionale Sirente Velino. Ente Parco Regionale Sirente Velino, Technical Relation
Nuñez MA, Hayward J, Horton TR, Amico GC, Dimarco RD, Barrios-Garcia MN, Simberloff D (2013) Exotic mammals disperse exotic fungi that promote invasion by exotic trees. PLoS One 8(6):e66832
Pacioni G, Bologna MA, Laurenzi M (1991) Insect attraction by Tuber: a chemical explanation. Mycol Res 95(12):1359–1363
Pacioni G, Rapino C, Zarivi O, Falconi A, Leonardi M, Battista N, Colafarina S, Sergi M, Bonfigli A, Miranda M, Barsacchi D, Maccarrone M (2015) Truffles contain endocannabinoid metabolic enzymes and anandamide. Phytochemistry 110:104–110
Pellegrini M, Febbo D, Pace A (1992) Segnalazioni di Istrice (Hystrix cristata) in Abruzzo. Atti della Società Italiana di Scienze Naturali, Museo Civico di Storia Naturale di Milano 132:359–363
Piattoni F, Ori F, Morara M, Iotti M, Zambonelli A (2012) The role of wild boars in spore dispersal of hypogeous fungi. Acta Mycol 47:145–153
Piattoni F, Amicucci A, Iotti M, Ori F, Stocchi V, Zambonelli A (2014) Viability and morphology of Tuber aestivum spores after passage through the gut of Sus scrofa. Fungal Ecol 9:52–56
Santini L (1980) The habits and influence on the environment of the old world porcupine Hystrix cristata L. in the northernmost part of its range. Vertebrate Pest Conference Proceedings Collection 149–153
Santoleri WM, Cerceo M (2007) Parco Nazionale della Majella. 30 itinerari scelti nel cuore della Montagna Madre. Edizioni Mediterranee, Roma
Schickmann S, Urban A, Kräutler K, Nopp-Mayr U, Hackländer K (2012) The interrelationship of mycophagous small mammals and ectomycorrhizal fungi in primeval, disturbed and managed Central European mountainous forests. Oecol 170:395–409
Song MS, Cao JZ, Yao YJ (2005) Occurrence of Tuber aestivum in China. Mycotaxon 91:75–80
Splivallo R, Culleré L (2016) The smell of truffles: from aroma biosynthesis to product quality. In: Zambonelli A, Iotti M, Murat C (eds) True truffles (Tuber spp.) in the world. Soil biology series, vol. 47. Springer International Publishing, Zurich, pp 393–407
Stobbe U, Egli S, Tegel W, Peter M, Sproll L, Büntgen U (2013) Potential and limitations of Burgundy truffle cultivation. Appl Microbiol Biotechnol 97(12):5215–5224
Trappe JM, Maser C (1976) Germination of spores of Glomus macrocarpus (Endogonaceae) after passage through a rodent digestive tract. Mycologia 67:433–436
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. USDA Forest Service. Pacific Northwest Research Station Gen. Tech. Rep.-GTR-772, Portland, OR
Trucchi E, Sbordoni V (2009) Unveiling an ancient biological invasion: molecular analysis of an old European alien, the crested porcupine (Hystrix cristata). BMC Evol Biol 9:109
Urban A (2016) Truffles and small mammals. In: Zambonelli A, Iotti M, Murat C (eds) True truffles (Tuber spp.) in the world. Soil biology series, vol. 47. Springer International Publishing, Zurich, pp 353–373
Vahdatzadeh M, Deveau A, Splivallo R (2013) The role of the microbiome of truffles in aroma formation: a meta-analysis approach. Appl Environ Microbiol 81(20):6946–6952
van Jaarsveld AS, Knight-Eloff AK (1984) Digestion in the porcupine Hystrix africaeaustralis. S Afr J Zool 19:109–112
Walker EP (1964) Mammals of the world. J Hopkins Press, Balt For 11:1004–1009
Wallis IR, Claridge AR, Trappe JM (2012) Nitrogen content, amino acid composition and digestibility of fungi from a nutritional perspective in animal mycophagy. Fungal Biol 116:590–602
Acknowledgements
We thank Professor Maurizio Biondi, zoologist at University of L’Aquila, for identification of faeces collected for this project.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Fig. 1S
Poor image of Hystrix cristata within the truffière, taken by Distianert 12MP 720P Infrared Camera (Shenzhen, CN), documenting its visits there. (TIF 4062 kb)
Rights and permissions
About this article
Cite this article
Ori, F., Trappe, J., Leonardi, M. et al. Crested porcupines (Hystrix cristata): mycophagist spore dispersers of the ectomycorrhizal truffle Tuber aestivum. Mycorrhiza 28, 561–565 (2018). https://doi.org/10.1007/s00572-018-0840-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00572-018-0840-1