Jump to ContentJump to Main Navigation
Show Summary Details
More options …


More options …
Volume 72, Issue 10


The porcupine as “Little Thumbling”: The role of Hystrix cristata in the spread of Helianthus tuberosus

Emiliano Mori / Giuseppe Mazza
  • Department of Biology, University of Florence, via Romana 17, 50125, Firenze, Italy
  • Consiglio per la ricerca in agricoltura e l’analisi dell’economia agraria (CREA), Research Centre for Plant Protection and Certification (CREA-DC), Via Lanciola 12/A, Cascine del Riccio, 50125, Firenze, Italy
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
/ Andrea Galimberti
  • ZooPlantLab, Department of Biotechnology and Biosciences, University of Milano-Bicocca, P.za della Scienza 2, 20126-I, Milano, Italy
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
/ Claudia Angiolini / Gianmaria Bonari
  • Department of Life Sciences, University of Siena, Via P.A. Mattioli, 4, 53100, Siena, Italy
  • Department of Botany and Zoology, Masaryk University, Kotlářská 2, CZ-61137, Brno, Czech Republic
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
Published Online: 2017-10-31 | DOI: https://doi.org/10.1515/biolog-2017-0136


The spread of alien invasive plants deserves strong and applied attention by conservation biologists, because it is regarded as one of the main causes of loss of native biodiversity. Herbivore species may be involved in the dispersal of invasive plants through zoochory. The Jerusalem artichoke Helianthus tuberosus is an invasive species in Europe, which has been introduced from North America and has shown a rapid spread in newly colonized areas. Crested porcupine Hystrix cristata mainly feed on this species (seeds and tubers) during its flowering period (i.e., late summer, early autumn) and it is suggested to be responsible for its spread through endozoochory. In this paper, the germination rate of the Jerusalem artichoke from faecal pellets of crested porcupines was analysed. Faecal pellets, collected between September and November 2016, were left to germinate at environmental conditions in sterile potting soil. After two weeks, germinated seedlings were genetically identified through DNA barcoding analyses. We reported the first case of endozoochory by the crested porcupine. The results showed a low germination rate (i.e., 16.7% out of 12 excrements), possibly because the digestive tract of crested porcupines affects the propagule viability. Despite this, the Jerusalem artichoke is showing a rapid and alarming increasing trend in our study area, suggesting that a potential role by wildlife may have been occurred. Given the high invasive potential of this plant species, further researches are required to assess and quantify the potential role of herbivores as dispersal agents.

This article offers supplementary material which is provided at the end of the article.

Key words: alien species; barcoding; crested porcupine; dispersal; endozoochory; Jerusalem artichoke

* Electronic supplementary material. The online version of this article (DOI: 10.1515/biolog-2017-0136) contains supplementary material, which is available to authorized users.


  • Agnew A.D.Q. & Flux J.E. 1970. Plant dispersal by hares (Lepus capensis L.) in Kenya. Ecology 51 (4): 735–737. CrossrefGoogle Scholar

  • Alkon P.U. 1999. Microhabitat to landscape impacts: crested porcupine digs in the Negev Desert highlands. J. Arid Environ. 41 (2): 183–202. CrossrefGoogle Scholar

  • Alkon P.U. & Olsvig-Whittaker L. 1989. Crested porcupine digs in the Negev desert highlands: patterns of density, size and longevity. J. Arid Environ. 17: 83–95.Google Scholar

  • Alkon P.U. & Saltz D. 1988. Foraging time and the northern range limits of Indian crested porcupines (Hystrix indica). J. Biogeogr. 15 (3): 403–408. CrossrefGoogle Scholar

  • Angiolini C., Landi M., Boddi M. & Frignani F. 2006. La vegetazione dell’alveo fluviale del sito d’importanza regionale torrente Trasubbie (Grosseto, Toscana meridionale). Atti della Società Toscana di Scienze Naturali, Memorie, Serie B 112: 127–151.Google Scholar

  • Barthelmess E. 2006. Hystrix africaeaustralis. Mammalian Species 788: 1–7.CrossrefGoogle Scholar

  • Bedini G., Pierini B., Roma-Marzio F., Caparelli K.F., Bonari G., Dolci D., Gestri G., D’Antraccoli M. & Peruzzi L. 2015. Wikiplantbase #Toscana, breaking the dormancy of floristic data. Plant Biosystems 150 (3): 601–610. CrossrefGoogle Scholar

  • Bertolino S., Colangelo P., Mori E. & Capizzi D. 2015. Good for management, not for conservation: an overview of research, conservation and management of Italian small mammals. Hystrix, Ital. J. Mammal. 26: 25–35. CrossrefGoogle Scholar

  • Boeken B., Schachak M., Gutterman Y. & Brand S. 1995. Patchiness and disturbance: plant community response to porcupine diggings in the central Negev. Ecography 18 (4): 410–422. CrossrefGoogle Scholar

  • Bonari G., Fajmon K., Malenovský I., Zelený D., Holuša J., Jongepierová I., Kočárek P., Konvička O., Uřičář J. & Chytrý M. 2017a. Management of semi-natural grasslands benefiting both plant and insect diversity: the importance of heterogeneity and tradition. Agricult. Ecosyst. Environ. 246: 243–252. CrossrefGoogle Scholar

  • Bonari G., Migliorini M., Landi M., Protano G., Fanciulli P.P. & Angiolini C. 2017b. Concordance between plant species, oribatid mites and soil in a Mediterranean stone pine forest. Arthropod-Plant Interactions 11 (1): 61–69. CrossrefGoogle Scholar

  • Bruno E. & Riccardi C. 1995. The diet of the crested porcupine Hystrix cristata L., 1758 in a Mediterranean rural area. Mammal. Biol. 60 (4): 226–236.Google Scholar

  • Burghardt K.T., Tallamy D.W. & Gregory Shriver W. 2009. Impact of native plants on bird and butterfly biodiversity in suburban landscapes. Conserv. Biol. 23 (1): 219–224. .CrossrefPubMedGoogle Scholar

  • Burrascano S., Copiz R., Del Vico E., Giarrizzo E., Mei M., Mortelliti A., Sabatini F.M. & Blasi C. 2015. Wild boar rooting intensity determines shifts in understorey composition and functional traits. Commun. Ecol. 16 (2): 244–253. CrossrefGoogle Scholar

  • Bustamante R., Simonetti J. & Mella J. 1992. Are foxes legitimate and efficient seed dispersers? A field test. Acta Oecol. 13: 203–208.Google Scholar

  • Camargo P.H., Martins M.M., Feitosa R.M. & Christianini A.V. 2016. Bird and ant synergy increases the seed dispersal effectiveness of an ornithochoric shrub. Oecologia 181 (2): 507– 518. CrossrefPubMedGoogle Scholar

  • Campos C.M., Campos V.E., Giannoni S.M., Rodriguez D., Albanese S. & Cona M.I. 2016. Role of small rodents in the seed dispersal process: Microcavia australis consuming Prosopis flexuosa fruits. Austral Ecol. 42 (1): 113–119. CrossrefGoogle Scholar

  • Campos C.M. & Ojeda R.A. 1997. Dispersal and germination of Prosopis flexuosa (Fabaceae) seeds by desert mammals in Argentina. J. Arid Environ. 35 (4): 707–714. CrossrefGoogle Scholar

  • Celesti-Grapow L., Alessandrini A., Arrigoni P.V., Banfi E., Bernardo L. & Bovio M. 2009. Inventory of the nonnative flora of Italy. Plant Biosyst. 143 (2): 386–430. CrossrefGoogle Scholar

  • Celesti-Grapow L., Pretto F., Carli E. & Blasi C. (eds). 2010. Flora vascolare alloctona e invasiva delle regioni d’Italia. Technical Report, Università “La Sapienza” di Roma, Roma, Italy, 208 pp. ISBN: 978-88-95814-33-9.Google Scholar

  • Clausen P., Nolet B.A., Fox A.D. & Klaassen M. 2002. Long-distance endozoochorous dispersal of submerged macrophyte seeds by migratory waterbirds in northern Europe-a critical review of possibilities and limitations. Acta Oecol. 23 (3): 191–203. CrossrefGoogle Scholar

  • Conti F., Abbate G., Alessandrini A. & Blasi C. (eds). 2005. An annotated checklist of the Italian vascular flora. Palombi Editors, Rome, Italy, 428 pp. ISBN: 88-7621-458-5.Google Scholar

  • Corsini M.T., Lovari S. & Sonnino S. 1995. Temporal activity patterns of crested porcupines Hystrix cristata. J. Zool. (Lond.) 236 (1): 43–54. CrossrefGoogle Scholar

  • Cosyns E., Claerbout S., Lamoot I. & Hoffmann M. 2005. Endozoochorous seed dispersal by cattle and horse in a spatially heterogeneous landscape. Plant Ecol. 178 (2): 149–162. CrossrefGoogle Scholar

  • de Villiers M.S. & van Aarde R.J. 1994. Aspects of habitat disturbance by Cape porcupines in a savanna ecosystem. South Afr. J. Zool. 29 (3): 217–220. CrossrefGoogle Scholar

  • Degn H.J. 1974. Feeding activity in the red squirrel (Sciurus vulgaris). J. Zool. (Lond.) 174 (4): 516–520. CrossrefGoogle Scholar

  • Euro+Med. 2006. Euro+Med PlantBase – the information resource for Euro-Mediterranean plant diversity. Published on the Internet http://ww2.bgbm.org/EuroPlusMed/ (accessed on the 25th October 2016).

  • Forget P.M. 1990. Seed-dispersal of Vouacapoua americana (Caesalpiniaceae) by caviomorph rodents in French Guiana. J. Trop. Ecol. 6 (4): 459–468. CrossrefGoogle Scholar

  • Forget P.M. & Milleron T. 1991. Evidence for secondary seed dispersal by rodents in Panama. Oecologia 87 (4): 596–599. CrossrefPubMedGoogle Scholar

  • Galimberti A., De Mattia F., Bruni I., Scaccabarozzi D., Sandionigi A., Barbuto M., Casiraghi M. & Labra M. 2014. A DNA barcoding approach to characterize pollen collected by honeybees. PloS One 9 (10): e109363. CrossrefPubMedGoogle Scholar

  • Galimberti A., Spinelli S., Bruno A., Mezzasalma V., Mattia F., Cortis P. & Labra M. 2016. Evaluating the efficacy of restoration plantings through DNA barcoding of frugivorous bird diets. Conserv. Biol. 30 (4): 763–773. .CrossrefPubMedGoogle Scholar

  • Gosper C.R., Stansbury C.D. & Vivian-Smith G. 2005. Seed dispersal of fleshy-fruited invasive plants by birds: contributing factors and management options. Divers. Distrib. 11 (6): 549–558. CrossrefGoogle Scholar

  • Green J.R. 1888. On the germination of the tuber of the Jerusalem Artichoke (Helianthus tuberosus). Ann. Bot. 1 (3/4): 223–236. CrossrefGoogle Scholar

  • Gutterman Y. 1997. Ibex diggings in the Negev Desert highlands of Israel as microhabitats for annual plants. Soil salinity, location and digging depth affecting variety and density of plant species. J. Arid Environ. 37 (4): 665–681. CrossrefGoogle Scholar

  • Gutterman Y., Golan T. & Garsani M. 1990. Porcupine diggings as a unique ecological system in a desert environment. Oecologia 85 (1): 122–127. CrossrefGoogle Scholar

  • Gutterman Y. & Herr N. 1981. Influence of porcupine (Hystrix indica) activity on the slopes of the Northern Negev mountains – germination and vegetation renewal in different geomorphological types and slope direction. Oecologia 51 (3): 332–334. CrossrefGoogle Scholar

  • Haskell J.P., Ritchie M.E. & Olff H. 2002. Fractal geometry predicts varying body size scaling relationships for mammal and bird home ranges. Nature 418: 527–530. CrossrefPubMedGoogle Scholar

  • Hämäläinen A., Broadley K., Droghini A., Haines J.A., Lamb C.T., Boutin S. & Gilbert S. 2017. The ecological significance of secondary seed dispersal by carnivores. Ecosphere 8 (2): e01685. CrossrefGoogle Scholar

  • Heinken T., Hanspach H., Raudnitschka D. & Schaumann F. 2002. Dispersal of vascular plants by four species of wild mammals in a deciduous forest in NE Germany. Phytocoenologia 32: 627–643.CrossrefGoogle Scholar

  • Heiser C.B., Smith D.M., Clevenger S.B. & Martin W.C. 1969. The North American sunflowers (Helianthus). Memoirs of the Torrey Botanical Club 22 (3): 1–218.Google Scholar

  • Hilley E. & Thiet R. 2015. Vulnerable broom crowberry (Corema conradii) benefits from ant seed dispersal in coastal US heathlands. Plant Ecol. 216 (8): 1091–1101. CrossrefGoogle Scholar

  • Izhaki I. & Ne’eman G. 1996. The effect of porcupine and bast scale on Aleppo pine recruitment after fire. Acta Oecol. 17 (2): 97–107.Google Scholar

  • Janzen D.H. 1986. Chihuahuan desert nopaleras defaunated big mammal vegetation. Annu. Rev. Ecol. Syst. 17: 595–636. CrossrefGoogle Scholar

  • Jaroszewicz B., Pirożnikow E. & Sondej I. 2013. Endozoochory by the guild of ungulates in Europe’s primeval forest. Forest Ecol. Manage. 305: 21–28. CrossrefGoogle Scholar

  • Jogloy S., Puttha R., Mikaew R., TulaW. & Kesmala T. 2006. Effect of propagated parts on percentage of emergence, growth and yield of Kaentawan (Helianthus tuberosus L.). Kaen Kaset. 1: http://agris.fao.org/agris-search/search.do?record (accessed 13.02.2017)

  • Kays S.J. & Nottingham S.F. 2007. Biology and Chemistry of Jerusalem Artichoke: Helianthus tuberosus L. CRC Press, London, UK, 496 pp. ISBN: 1420044958, 9781420044959Google Scholar

  • Khan A.A., Ahmad S., Hussain I. & Munir S. 2000. Deterioration impact of Indian crested porcupine, Hystrix indica, on forestry and agricultural systems in Pakistan. Int. Biodeterior. Biodegr. 45 (3-4): 143–149. CrossrefGoogle Scholar

  • Landi M., Angiolini C. & De Dominicis V. 2002. Analisi fitosociologica dei fiumi della Toscana meridionale: il tratto mediobasso del Merse (Italia centrale). Stud. Bot. 21: 37–88.Google Scholar

  • Landi M., Zoccola A., Gonnelli V., Lastrucci L., Saveri C., Quilghini G., Bottacci A. & Angiolini C. 2014. Effect of grazing on the population of Matteuccia struthiopteris at the southern limit of its distribution in Europe. Plant Sp. Biol. 31: 3–10. CrossrefGoogle Scholar

  • Laurenzi A., Bodino N. & Mori E. 2016. Much ado about nothing: assessing the impact of a problematic rodent on agriculture and native trees. Mammal Res. 61 (1): 65–72. CrossrefGoogle Scholar

  • Lima I.P., Nogueira M.R., Monteiro L.R. & Peracchi A.L. 2016. Frugivoria e dispersăo de sementes por morcegos na Reserva Natural Vale, Sudeste do Brasil, pp. 433–452. In: Rolim S.G, de Menezes L.F.T. & Srbek-Araujo A.C (eds), Floresta Atlantica de Tabuleiro: diversidade e endemismos na Reserva Natural Vale, Editora Rupreste, Sao Paulo, 496 pp. ISBN: 978-85-62805-63-9Google Scholar

  • Lovari S., Corsini M.T., Guazzini B., Romeo G. & Mori E. 2017. Suburban ecology of the crested porcupine in a heavily poached area: a global approach. Eur. J. Wildl. Res. 63: 10. CrossrefGoogle Scholar

  • Menchetti M. & Mori E. 2014. Worldwide impact of alien parrots (Aves Psittaciformes) on native biodiversity and environment: a review. Ethol. Ecol. Evol. 26 (2-3): 172–194. CrossrefGoogle Scholar

  • Mori E., Bozzi R. & Laurenzi A. 2017. Feeding habits of the crested porcupine Hystrix cristata L. 1758 (Mammalia, Rodentia) in a Mediterranean area of Central Italy. Eur. Zool. J. 84 (1): 261–265. CrossrefGoogle Scholar

  • Mori E. & Lovari S. 2014. Sexual size monomorphism in the crested porcupine (Hystrix cristata). Mammal. Biol. 79 (2): 157–160. CrossrefGoogle Scholar

  • Mori E., Mazzoglio P.J., Rima P.C., Aloise G. & Bertolino S. 2015. Bark-stripping damage by Callosciurus finlaysonii introduced into Italy. Mammalia 80 (5): 507–514. CrossrefGoogle Scholar

  • Mori E., Menchetti M., Dondini G., Biosa D. & Vergari S. 2014a. Theriofauna of Site of Community Importance Poggi di Prata (Grosseto, Central Italy): Terrestrial mammals and preliminary data on Chiroptera. Check List 10 (4): 718–723. CrossrefGoogle Scholar

  • Mori E., Nourisson D.H., Lovari S., Romeo G. & Sforzi A. 2014b. Self-defence may not be enough: moonlight avoidance in a large, spiny rodent. J. Zool. (Lond.) 294 (1): 31–40. CrossrefGoogle Scholar

  • Mori E., Sforzi A. & Di Febbraro M. 2013. From the Apennines to the Alps: recent range expansion of the crested porcupine Hystrix cristata L., 1758 (Mammalia: Rodentia: Hystricidae) in Italy. Ital. J. Zool. 80 (4): 469–480. CrossrefGoogle Scholar

  • Myers J.A., Vellend M., Gardescu S. & Marks P.L. 2004. Seed dispersal by white-tailed deer: implications for long-distance dispersal, invasion, and migration of plants in eastern North America. Oecologia 139 (1): 35–44. CrossrefPubMedGoogle Scholar

  • Peruzzi L. & Bedini G. 2015. Wikiplantbase #Toscana v2.1. Available at: http://bot.biologia.unipi.it/wpb/toscana/index.html. (accessed 09.02.2017)

  • Pigozzi G. 1988. Quill-marking, a method to identify crested porcupines individually. Acta Theriol. 33 (11): 138–142.CrossrefGoogle Scholar

  • Pigozzi G. 1992. Frugivory and seed dispersal by the European badger in a Mediterranean habitat. J. Mammal. 73 (3): 630–639. CrossrefGoogle Scholar

  • Pimentel D., Zuniga R. & Morrison D. 2005. Update on the environmental and economic costs associated with alien-invasive species in the United States. Ecol. Econom. 52 (3): 273–288. CrossrefGoogle Scholar

  • Podda L., Santo A., Leone C., Mayoral O. & Bacchetta G. 2017. Seed germination, salt stress tolerance and seedling growth of Opuntia ficus-indica (Cactaceae), invasive species in the Mediterranean Basin. Flora 229: 50–57. CrossrefGoogle Scholar

  • Richardson D.M., Pyšek P., Rejmanek M., Barbour M.G., Panetta F.D. & West C.J. 2000. Naturalization and invasion of alien plants: concepts and definitions. Divers. Distrib. 6 (2): 93–107. CrossrefGoogle Scholar

  • Santo A., Mattana E. & Bacchetta G. 2015. Inter- and intraspecific variability in seed dormancy loss and germination requirements in the Lavatera triloba aggregate (Malvaceae). Plant Ecol. Evol. 148 (1): 100–110. CrossrefGoogle Scholar

  • Selvi F. 2010. A critical checklist of the vascular flora of Tuscan Maremma (Grosseto province, Italy). Flora Mediterr. 20: 47–139.Google Scholar

  • Sharma D. & Prasad S.N. 1992. Tree debarking and habitat use by porcupine (Hystrix indica Kerr) in Sariska National Park in Western India. Mammalia 56 (3): 351–362. CrossrefGoogle Scholar

  • Sherbrooke W.C. 1976. Differential acceptance of toxic jojoba seeds (Simmondsia chinensis) by four Sonoran desert Heteromyd rodents. Ecology 57 (3): 569–602. CrossrefGoogle Scholar

  • Simberloff D. & Von Holle B. 1999. Positive interactions of nonindigenous species: invasional meltdown? Biol. Invas. 1 (1): 21–32. CrossrefGoogle Scholar

  • Starfinger U., Edwards K., Kowarik I. & Williamson M. 1998. Plant Invasions: Ecological Mechanisms and Human Responses. Backhuys Publishers, Leiden, The Netherlands, 368 pp. ISBN-10: 9057820056, ISBN-13: 978-9057820052Google Scholar

  • Tallamy D.W. 2004. Do alien plants reduce insect biomass? Conserv. Biol. 18 (6): 1689–1692. CrossrefGoogle Scholar

  • Tella J.T., Bañnos-Villalba A., Hernàndez-Brito D., Rojas A., Pacifico E.C., Dìaz-Luque J.A., Carrete M., Blanco G. & Hiraldo F. 2015. Parrots as overlooked seed dispersers. Front. Ecol. Environ. 13 (6): 338–339. CrossrefGoogle Scholar

  • Trucchi E., Facon B., Gratton P., Mori E., Stenseth N.C. & Jentoft S. 2016. Long live the alien: is high genetic diversity a pivotal aspect of crested porcupine (Hystrix cristata) longlasting and successful invasion? Mol. Ecol. 25 (15): 3527–3539. .CrossrefGoogle Scholar

  • Turbè A., Strubbe D., Mori E., Carrete M., Chiron F., Clergeau P., Gonzalez-Moreno P., Le Louarn M., Luna A., Menchetti M., NentwigW., Parau L.G., Postigo J.L., RabitschW., Senar J.C., Tollington S., Vanderhoeven S., Weiserbs A. & Shwartz A. 2017. Assessing the assessments: evaluation of four impact assessment protocols for invasive alien species. Divers. Distrib. 23 (3): 297–307. CrossrefGoogle Scholar

  • Vander Wall S.B. 1990. Food hoarding in animals. University of Chicago Press, Chicago, Illinois, USA, 455 pp. ISBN-10: 0226847357Google Scholar

  • Weber E. & Gut D. 2004. Assessing the risk of potentially invasive plant species in central Europe. J. Nat. Conserv. 12 (3): 171–179. CrossrefGoogle Scholar

  • Weber E., Sun S.G. & Li B. 2008. Invasive alien plants in China: diversity and ecological insights. Biol. Invas. 10 (8): 1411–1429. CrossrefGoogle Scholar

  • Yair A. & Shashak M. 1987. Studies in watershed ecology of an arid area, pp. 145–193. In: Berkofsky L. & Wurtle M. (eds), Progress in Desert Research, Rowman and Littlefield (Eds.), Totowa, New Jersey, USA, 368 pp. ISBN-13: 978-0847674800, ISBN-10: 0847674800Google Scholar

About the article

Received: 2017-04-28

Accepted: 2017-07-08

Published Online: 2017-10-31

Published in Print: 2017-10-26

Citation Information: Biologia, Volume 72, Issue 10, Pages 1211–1216, ISSN (Online) 1336-9563, ISSN (Print) 0006-3088, DOI: https://doi.org/10.1515/biolog-2017-0136.

Export Citation

© 2017 Institute of Zoology, Slovak Academy of Sciences.Get Permission

Supplementary Article Materials

Citing Articles

Here you can find all Crossref-listed publications in which this article is cited. If you would like to receive automatic email messages as soon as this article is cited in other publications, simply activate the “Citation Alert” on the top of this page.


Comments (0)

Please log in or register to comment.
Log in