Wild boar rooting intensity determines shifts in understorey composition and functional traits

Abstract

In recent decades, the European populations of wild boar have grown substantially, as has the impact of this species, owing above all to its rooting activity. Our aim was to investigate the relationships between vascular plant understorey and wild boar rooting intensity. The questions we addressed are: does rooting intensity influence understorey species composition and diversity? Which functional traits are associated with different levels of rooting? We performed a comparative analysis of plant communities in areas with contrasting levels of rooting intensity within a Mediterranean deciduous lowland forest in central Italy. Besides comparing species composition and diversity, we tested the association between species traits and rooting levels through fourth-corner analysis. We found that contrasting levels of rooting were associated to different understorey species composition and evenness, while we observed no significant difference in species richness. In contrast with our expectations, sites with lower rooting returned i) lower evenness values and ii) a higher proportion of species characterized by traits related to resistance or response to herbivory, i.e., spinescence, clonality, endozoochory, underground storage organs, and low height values. Our findings suggest that current vegetation patterns partly depend on the legacy effect of past rooting disturbance, since the areas currently subjected to low rooting intensity were likely to be intensely rooted in the past. These areas may have developed a marked dominance of clonal thorny species that, in turn, inhibited further feeding activities by wild boar.

References

  1. Abbate, G., S. Bonacquisti, S. Burrascano, E. Giovi, A. Giuliani, F. Pretto and E. Scassellati. 2015. Woody flora as a predictor of vascular plant richness: An insight in Italy. Plant Biosyst. 149: 565–573.

    Article  Google Scholar 

  2. Anderson, M.J. 2001. A new method for non-parametric multivariate analysis of variance. Austral. Ecol. 26: 32–46.

    Google Scholar 

  3. Avery, E.T. and E.H. Burkhart. 2002. Forest Measurements. 5th ed. McGraw-Hill Higher Education, New York, N Y.

    Google Scholar 

  4. Ballari, S.A. and M.N. Barrios-Garcia. 2014. A review of wild boar Sus scrofa diet and factors affecting food selection in native and introduced ranges. Mammal. Rev. 44: 124–134.

    Article  Google Scholar 

  5. Barrios-Garcia, M.N. and S.A. Ballari. 2012. Impact of wild boar (Sus scrofa) in its introduced and native range: a review. Biol. Invasions 14: 2283–2300.

    Article  Google Scholar 

  6. Bieber, C. and T. Ruf. 2005. Population dynamics in wild boar Sus scrofa: ecology, elasticity of growth rate and implications for the management of pulsed resource consumers. J. Appl. Ecol. 42: 1203–1213.

    Article  Google Scholar 

  7. Blasi, C., G. Capotorti, R. Copiz, D. Guida, B. Mollo, D. Smiraglia, and L. Zavattero. 2014. Classification and mapping of the ecore-gions of Italy. Plant Biosyst. 148: 1255–1345.

    Article  Google Scholar 

  8. Blasi, C., L. Filesi, A. Stanisci, R. Frondoni, R. Di Pietro, and M. L. Carranza. 2002. Excursion to the Circeo National Park. Fitosociologia 39: 91–130.

    Google Scholar 

  9. Boitani, L., L. Mattei, D. Nonis and F. Corsi. 1994. Spatial and activity patterns of wild boars in Tuscany, Italy. J. Mammal. 75: 600–612.

    Article  Google Scholar 

  10. Bratton, S.P. 1975. The Effect of the European Wild Boar, Sus scrofa, on Gray Beech Forest in the Great Smoky Mountains. Ecology 56: 1356–366.

    Article  Google Scholar 

  11. Brooker, R.W., F.T. Maestre, R.M. Callaway, C.L. Lortie, L.A. Cavieres, G. Kunstler, P. Liancourt, K. Tielboerger, J.M.J. Travis, F. Anthelme, C. Armas, L. Coll, E. Corcket, S. Delzon, E. Forey, Z. Kikvidze, J. Olofsson, F.I. Pugnaire, C.L. Quiroz, P. Saccone, K. Schiffers, M. Seifan, B. Touzard and R. Michalet. 2008. Facilitation in plant communities: the past, the present, and the future. J. Ecol. 96: 18–34.

    Google Scholar 

  12. Burrascano, S., F.M. Sabatini and C. Blasi. 2011. Testing indicators of sustainable forest management on understorey composition and diversity in southern Italy through variation partitioning. Plant Ecol. 212: 829–841.

    Article  Google Scholar 

  13. Burrascano, S., E. Giarrizzo, S. Bonacquisti, R. Copiz, E. Del Vico, S. Fagiani, A. Mortelliti and C. Blasi. 2015. Quantifying Sus scrofa rooting effects on the understorey of the deciduous broadleaf forests in Castelporziano Estate (Italy). Rendiconti Lincei. 26, Suppl. 3: 317–324.

    Article  Google Scholar 

  14. Catorci, A., R. Gatti and S. Cesaretti. 2012. Effect of sheep and horse grazing on species and functional composition of sub-Mediterranean grasslands. Appl. Veg. Sci. 15: 459–469.

    Article  Google Scholar 

  15. Catorci, A., S. Cesaretti and F.M. Tardella. 2014. Effect of tall-grass invasion on the flowering-related functional pattern of submedi-terranean hay-meadows. Plant Biosyst. 148: 1127–1137.

    Article  Google Scholar 

  16. Champagnon, J., J. Elmberg, M. Guillemain, M. Gauthier-Clerc and J.D. Lebreton. 2012. Conspecifics can be aliens too: A review of effects of restocking practices in vertebrates. J. Nat. Conserv. 20: 231–241.

    Article  Google Scholar 

  17. Conti, F., G. Abbate, A. Alessandrini and C. Blasi. 2005. An annotated checklist of Italian vascular flora, 1st edn. Palombi Editore, Roma.

  18. Cornelissen, J.H.C., S. Lavorel, E. Garnier, S. Diaz, N. Buchmann, D.E. Gurvich, P.B. Reich, H. ter Steege, H.D. Morgan, M.G.A. van der Heijden, J.G. Pausas and H. Poorter. 2003. A handbook of protocols for standardised and easy measurement of plant functional traits worldwide. Aust. J. Bot. 51: 335–380.

    Article  Google Scholar 

  19. Cuevas, M.F., A. Novillo, C. Campos, M.A. Dacar and R.A. Ojeda. 2010. Food habits and impact of rooting behaviour of the invasive wild boar, Sus scrofa, in a protected area of the Monte Desert, Argentina. J. Arid Environ. 74: 1582–1585.

    Article  Google Scholar 

  20. Cushman, J.H., T.A. Tierney and J.M. Hinds. 2004. Variable effects of feral pig disturbances on native and exotic plants in a California grassland. Ecol. Appl. 14: 1746–1756.

    Article  Google Scholar 

  21. Debussche, M., G. Debussche and J. Lepart. 2001. Changes in the vegetation of Quercus pubescens woodland after cessation of coppicing and grazing. J. Veg. Sci. 12: 81–92.

    Article  Google Scholar 

  22. Dowgiallo, G. and D. Bottini. 1998. Aspetti pedologici del Parco Nazionale del Circeo. In: A. Stanisci and S. Zerunian (eds), Flora e Vegetazine del Parco Nazionale del Circeo. Ministero per le Politiche Agricole, gestione ex A.S.F.D., Sabaudia. pp. 33–46.

  23. Dray, S. and A.B. Dufour. 2007. The ade4 package: implementing the duality diagram for ecologists. J. Stat. Softw. 22: 1–20.

    Article  Google Scholar 

  24. Dray, S. and P. Legendre. 2008. Testing the species traits-environment relationships: the fourth-corner problem revisited. Ecology 89: 3400–3412.

    Article  PubMed  PubMed Central  Google Scholar 

  25. Dufrêne, M. and P. Legendre. 1997. Species assemblages and indicator species: the need for a flexible asymmetrical approach. Ecol. Monogr. 61: 345–366.

    Google Scholar 

  26. Fagiani, S., D. Fipaldini, L. Santarelli, S. Burrascano, E. Del Vico, E. Giarrizzo, M. Mei, A.V. Taglianti, L. Boitani and A. Mortelliti. 2014. Monitoring protocols for the evaluation of the impact of wild boar (Sus scrofa) rooting on plants and animals in forest ecosystems. Hystrix 25: 31–38.

    Google Scholar 

  27. Gilliam, F.S. 2007. The ecological significance of the herbaceous layer in temperate forest ecosystems. Bioscience 57: 845–858.

    Article  Google Scholar 

  28. Gomez, J.M. and J.A. Hodar. 2008. Wild boars (Sus scrofa) affect the recruitment rate and spatial distribution of holm oak (Quercus ilex). For. Ecol. Manag. 256: 1384–1389.

    Article  Google Scholar 

  29. Haaverstad, O., O. Hjeljord and H.K. Wam. 2014. Wild boar rooting in a northern coniferous forest - minor silviculture impact. Scand. J. Forest Res. 29: 90–95.

    Article  Google Scholar 

  30. Heinken, T., M. Schmidt, G. von Oheimb, W.U. Kriebitzsch and H. Ellenberg. 2006. Soil seed banks near rubbing trees indicate dispersal of plant species into forests by wild boar. Basic Appl. Ecol. 7: 31–44.

    Article  Google Scholar 

  31. Hone, J. 2002. Feral pigs in Namadgi National Park, Australia: dynamics, impacts and management. Biol. Conserv. 105: 231–242.

    Article  Google Scholar 

  32. Hunter, M.L. 1990. Wildlife, Forests and Forestry: Principles of Managing Forests for Biological Diversity. Prentice Hall, Englewood Cliffs.

  33. Ickes, K., C.J. Paciorek and S.C. Thomas. 2005. Impacts of nest construction by native pigs (Sus scrofa) on lowland Malaysian rain forest saplings. Ecology 86: 1540–1547.

    Article  Google Scholar 

  34. Kattge, J., S. Diaz, S. Lavorel, C. Prentice, P. Leadley et al. 2011. TRY - a global database of plant traits. Global Change Biol. 17: 2905–2935.

    Article  Google Scholar 

  35. Keddy, P.A. 1992. Assembly and response rules - 2 goals for predictive community ecology. J. Veg. Sci. 3: 157–164.

    Article  Google Scholar 

  36. Kleyer, M., R.M. Bekker, I.C. Knevel, J.P. Bakker, K. Thompson, M. Sonnenschein, P. Poschlod, J.M. van Groenendael, L. Klimes, J. Klimesova, S. Klotz, G.M. Rusch, M. Hermy, D. Adriaens, G. Boedeltje, B. Bossuyt, A. Dannemann, P. Endels, L. Gotzenberger, J.G. Hodgson, A.K. Jackel, I. Kuhn, D. Kunzmann, W.A. Ozinga, C. Romermann, M. Stadler, J. Schlegelmilch, H. J. Steendam, O. Tackenberg, B. Wilmann, J.H.C. Cornelissen, O. Eriksson, E. Garnier and B. Peco. 2008. The LEDA Traitbase: a database of life-history traits of the Northwest European flora. J. Ecol. 96: 1266–1274.

    Article  Google Scholar 

  37. Klimesova, J. and F. de Bello. 2009. CLO-PLA: the database of clonal and bud bank traits of Central European flora. J. Veg. Sci. 20: 511–516.

    Article  Google Scholar 

  38. Lavorel, S., S. Díaz, J.H.C. Cornelissen, E. Garnier, S.P. Harrison, S. McIntyre, J.G. Pausas, N. Pérez-Harguindeguy, C. Roumet and C. Urcelay. 2007. Plant Functional Types: Are We Getting Any Closer to the Holy Grail? In: J. Canadell, D. Pataki and L. Pitelka (eds), Terrestrial Ecosystems in a Changing World. Springer-Verlag, Berlin Heidelberg. pp. 149–164.

    Chapter  Google Scholar 

  39. Lavorel, S. and E. Garnier. 2002. Predicting changes in community composition and ecosystem functioning from plant traits: revisiting the Holy Grail. Funct. Ecol. 16: 545–556.

    Article  Google Scholar 

  40. Li, L.L., J.B. Shi, J. Wang, Y.M. Gao, L.B. Wang, J.Q. Wang and X. Ying. 2013. Factors influencing wild boar damage in Taohongling National Nature Reserve in China: a model approach. Eur. J. Wildl. Res. 59: 179–184.

    Article  Google Scholar 

  41. Ma, M., X. Zhou and G. Du. 2013. Effects of disturbance intensity on seasonal dynamics of alpine meadow soil seed banks on the Tibetan Plateau. Plant Soil 369: 283–295.

    Article  CAS  Google Scholar 

  42. Martinez-Palle, E. and G. Aronne. 1999. Flower development and reproductive continuity in Mediterranean Ruscus aculeatus L. (Liliaceae). Protoplasma 208: 58–64.

    Article  Google Scholar 

  43. Massei, G. and P. Genov. 2004. The environmental impact of wild boar. Galemys 16: 135–145.

    Google Scholar 

  44. Nuttle, T., T.E. Ristau and A.A. Royo. 2014. Long-term biological legacies of herbivore density in a landscape-scale experiment: forest understoreys reflect past deer density treatments for at least 20 years. J. Ecol. 102: 221–228.

    Article  Google Scholar 

  45. Ohashi, H., M. Saito, R. Horie, H. Tsunoda, H. Noba, H. Ishii, T. Kuwabara, Y. Hiroshige, S. Koike, Y. Hoshino, H. Toda and K. Kaji. 2013. Differences in the activity pattern of the wild boar Sus scrofa related to human disturbance. Eur. J. Wildl. Res. 59: 167–177.

    Article  Google Scholar 

  46. Onaindia, M., I. Dominguez, I. Albizu, C. Garbisu and I. Amezaga. 2004. Vegetation diversity and vertical structure as indicators of forest disturbance. For. Ecol. Manag. 195: 341–354.

    Article  Google Scholar 

  47. Paušič, A. and A. Čarni. 2013. Records of past land use are best stored in soil properties. Plant Biosyst. 147: 654–663.

    Article  Google Scholar 

  48. Perea, R. and L. Gil. 2014. Tree regeneration under high levels of wild ungulates: The use of chemically vs. physically-defended shrubs. For. Ecol. Manag. 312: 47–54.

    Article  Google Scholar 

  49. Pignatti, S. 1982. Flora d’Italia. Edagricole, Bologna.

  50. Pinna, W., G. Nieddu, G. Moniello and M.G. Cappai. 2007. Vegetable and animal food sorts found in the gastric content of Sardinian Wild Boar (Sus scrofa meridionalis). J. Anim. Physiol. Anim. Nutr. 91: 252–255.

    Article  CAS  Google Scholar 

  51. Royo, A.A. and W.P. Carson. 2006. On the formation of dense under-story layers in forests worldwide: consequences and implications for forest dynamics, biodiversity, and succession. Can. J. For. Res. 36: 1345–1362.

    Article  Google Scholar 

  52. Sabatini, F.M., S. Burrascano, H. Tuomisto and C. Blasi. 2014a. Ground layer plant species turnover and beta diversity in Southern-European old-growth forests. PLoS ONE 9: e95244.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Sabatini, F.M., J.I. Burton, R.M. Scheller, K.L. Amatangelo and D.J. Mladenoff. 2014b. Functional diversity of ground-layer plant communities in old-growth and managed northern hardwood forests. Appl. Veg. Sci. 17: 398–407.

    Article  Google Scholar 

  54. Saezroyuela, C. and J.L. Telleria. 1986. The increased population of the wild boar (Sus scrofa L.) in Europe. Mammal. Rev. 16: 97– 101.

    Article  Google Scholar 

  55. Sandom, C.J., J. Hughes and D.W. Macdonald. 2013. Rewilding the Scottish Highlands: Do wild boar, Sus scrofa, use a suitable foraging strategy to be effective ecosystem engineers? Restor. Ecol. 21: 336–343.

    Article  Google Scholar 

  56. Schley, L., M. Dufrene, A. Krier and A.C. Frantz. 2008. Patterns of crop damage by wild boar (Sus scrofa) in Luxembourg over a 10-year period. Eur. J. Wildl. Res. 54: 589–599.

    Article  Google Scholar 

  57. Schmidt, M., K. Sommer, W.U. Kriebitzsch, H. Ellenberg and G. von Oheimb. 2004. Dispersal of vascular plants by game in northern Germany. Part I: Roe deer (Capreolus capreolus) and wild boar (Sus scrofa). Eur. J. Forest Res. 123: 167–176.

    Article  Google Scholar 

  58. Siemann, E., J.A. Carrillo, C.A. Gabler, R. Zipp and W.E. Rogers. 2009. Experimental test of the impacts of feral hogs on forest dynamics and processes in the southeastern US. For. Ecol. Manag. 258: 546–553.

    Article  Google Scholar 

  59. Sims, N.K., E.A. John and A.J.A. Stewart. 2014. Short-term response and recovery of bluebells (Hyacinthoides non-scripta) after rooting by wild boar (Sus scrofa). Plant Ecol. 215: 1409–1416.

    Article  Google Scholar 

  60. Valenzuela, A.E.J., C.B. Anderson, L. Fasola and J.L. Cabello. 2014. Linking invasive exotic vertebrates and their ecosystem impacts in Tierra del Fuego to test theory and determine action. Acta Oecol. 54: 110–118.

    Article  Google Scholar 

  61. Van Reeuwijk, L.P. (ed.). 2002. Procedures for Soil Analysis, 6th edition. Tech. Pap. 9, ISRIC. Wageningen.

  62. Višnjić, Ć., S. Solaković, F. Mekić, B. Balić, S. Vojniković, M. Dautbašić, S. Gurda, F. Ioras, J. Ratnasingam and I.V. Abrudan. 2013. Comparison of structure, regeneration and dead wood in virgin forest remnant and managed forest on Grmeč Mountain in Western Bosnia. Plant Biosyst. 147: 913–922.

    Article  Google Scholar 

  63. Welander, J. 2000. Spatial and temporal dynamics of wild boar (Sus scrofa) rooting in a mosaic landscape. J. Zool. 252: 263–271.

    Article  Google Scholar 

  64. Wirthner, S., M. Schutz, D.S. Page-Dumroese, M.D. Busse, J.W. Kirchner and A.C. Risch. 2012. Do changes in soil properties after rooting by wild boars (Sus scrofa) affect understory vegetation in Swiss hardwood forests? Can. J. For. Res. 42: 585–592.

    Article  CAS  Google Scholar 

  65. Wright, I.J., P.B. Reich, M. Westoby, D.D. Ackerly, Z. Baruch, F. Bongers, J. Cavender-Bares, T. Chapin, J.H.C. Cornelissen, M. Diemer, J. Flexas, E. Garnier, P.K. Groom, J. Gulias, K. Hikosaka, B.B. Lamont, T. Lee, W. Lee, C. Lusk, J.J. Midgley, M.L. Navas, U. Niinemets, J. Oleksyn, N. Osada, H. Poorter, P. Poot, L. Prior, V.I. Pyankov, C. Roumet, S.C. Thomas, M.G. Tjoelker, E.J. Veneklaas and R. Villar. 2004. The worldwide leaf economics spectrum. Nature 428: 821–827.

    Article  CAS  Google Scholar 

  66. Zerunian S. 2005. Studio di fattibilità per la reintroduzione di specie significative e gestione sostenibile del cinghiale nel Parco Nazionale del Circeo, Contributo di Ricerca con atto del 02 Febbraio 2005. Parco Nazionale del Circeo.

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Burrascano, S., Copiz, R., Del Vico, E. et al. Wild boar rooting intensity determines shifts in understorey composition and functional traits. COMMUNITY ECOLOGY 16, 244–253 (2015). https://doi.org/10.1556/168.2015.16.2.12

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Keywords

  • Circeo National Park
  • Deciduous oak forest
  • Fourth-corner analysis
  • Indicator Species Analysis
  • Ruscus aculeatus
  • Sus scrofa

Nomenclature for plants

  • Conti et al. (2005)