Skip to main content

Lepidoptera Papilionoidea communities as a sentinel of biodiversity threat: the case of wild boar rooting in a Mediterranean habitat

Abstract

Butterfly communities can be modified by the activities of large mammals. The wild boar (Sus scrofa) is one of the most common mammals in Europe and has notably expanded its distribution range in recent decades. The present work aimed to investigate the possible effect of wild boar rooting activity on butterflies in olive groves inside the “Cilento, Vallo di Diano and Alburni” National Park. Butterflies were surveyed in five Rooted (R) and five Control areas (C). Transects were made from April to September in 2011 and 2012. Forty-three species and 3659 individuals were found, of which 39 species and 2426 individuals were detected in C areas and 31 species and 1233 individuals in R areas. A community-level approach showed a significantly higher abundance, richness and Shannon–Wiener index in C than in R. An ecological-level approach indicated that more specialised butterflies were significantly more affected by wild boar activity. Finally, the response of single species was investigated: two species (Colias croceus and Polyommatus icarus) were significantly more represented in R, whereas six species (Aricia agestis, Hipparchia statilinus, Lasiommata megera, Melanargia arge, Pyronia cecilia and Thymelicus acteon) were significantly more abundant in C. Three species considered at risk (M. arge; Annex II of Directive 92/43/EEC; H. statilinus and T. acteon: European Red List) were less represented in rooted areas. Overall, the intensive wild boar activity negatively correlated with butterflies in the olive groves studied.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2

References

  • Abaigar T, del Barrio G, Vericad JR (1994) Habitat preference of wild boar (Sus scrofa L, 1758) in a Mediterranean environment. Indirect evaluation by signs. Mammalia 58:201–210

    Article  Google Scholar 

  • Acevedo P, Escudero MA, Muñóz R, Gortázar C (2006) Factors affecting wild boar abundance across an environmental gradient in Spain. Acta Theriol 51(3):327–336

    Article  Google Scholar 

  • Andrzejewski R, Jezierski W (1978) Management of the wild boar population and its effect on commercial land. Acta Theriol 23:309–333

    Article  Google Scholar 

  • Apollonio M, Anderson R, Putman R (2010) European ungulates and their management in the 21st century. Cambridge University Press, Cambridge

    Google Scholar 

  • Baber DW, Coblentz BE (1987) Diet, nutrition, and conception in feral pigs of Santa Catalina Island. J Wildl Manage 51:306–317

    Article  Google Scholar 

  • Barrios-Garcia MN, Ballari SA (2012) Impact of wild boar (Sus scrofa) in its introduced and native range: a review. Biol Invasion 14:2283–2300

    Article  Google Scholar 

  • Bonal R, Muñoz A (2007) Multi-trophic effects of ungulate intraguild predation on acorn weevils. Oecologia 152:533–540

    Article  PubMed  Google Scholar 

  • Börschig C, Klein AM, von Wehrden H, Krauss J (2013) Traits of butterfly communities change from specialist to generalist characteristics with increasing land-use intensity. Basic Appl Ecol 14:547–554

    Article  Google Scholar 

  • Brangi A, Meriggi A (2003) Espansione del Cinghiale (Sus scrofa) e danni alle coltivazioni in un’area delle Prealpi occidentali. Hystrix 14:1–2

    Google Scholar 

  • Bratton SP (1974) The effect of the European wild boar (Sus scrofa) on the high-elevation vernal flora in Great Smoky Mountains National Park. B Torrey Bot Club 101:198–206

    Article  Google Scholar 

  • Bratton SP, Harmon ME, White PS (1982) Patterns of European wild boar rooting in the western Great Smoky Mountains. Castanea 47:230–242

    Google Scholar 

  • Braza F, Alvarez F (1989) Utilisation de l’habitat et organisation sociale du sanglier (Sus scrofa L.) à Doñana (Sud-Ouest de l’Espagne). Can J Zool 67(8):2047–2051

    Article  Google Scholar 

  • Bueno CG, Alados CL, Gómez-García D, Barrio IC, García-González R (2009) Understanding the main factors in the extent and distribution of wild boar rooting on alpine grasslands. J Zool 279:195–202

    Article  Google Scholar 

  • Calenge C, Maillard D, Fournier P, Fouque C (2004) Efficiency of spreading maize in the gariques to reduce wild boar (Sus scrofa) damage to Mediterrean vineyards. Eur J Wildl Res 50:112–120

    Google Scholar 

  • Clausen HD, Holbeck HB, Reddersen J (2001) Factors influencing abundance of butterflies and burnet moths in the uncultivated habitats of an organic farm in Denmark. Biol Conserv 98:167–178

    Article  Google Scholar 

  • Clavel J, Julliard R, Devictor V (2010) Worldwide decline of specialist species: toward a global functional homogeneization? Front Ecol Environ 9:222–228

    Article  Google Scholar 

  • Cleary DFR, Genner MJ (2004) Changes in rain forest butterfly diversity following major ENSO-induced fires in Borneo. Glob Biogeogr 13:129–140

    Article  Google Scholar 

  • Courchamp F, Chapuis JL, Pascal M (2003) Mammal invaders on islands: impact, control and control impact. Biol Rev 78:347–383

    Article  PubMed  Google Scholar 

  • D’Aniello B, Stanislao I, Bonelli S, Balletto E (2011) Haying and grazing effects on the butterfly communities of two Mediterranean-area grasslands. Biodiv Conserv 20:1731–1744

    Article  Google Scholar 

  • Dardaillon M (1986) Seasonal variations in habitat selection and spatial distribution of wild boar (Sus scrofa) in the Camargue, Southern France. Behav Process 13(3):251–268

    CAS  Article  Google Scholar 

  • Davis JD, Debinski DM, Danielson BJ (2007) Local and landscape effects on the butterfly community in fragmented Midwest USA prairie habitats. Landsc Ecol 22(9):1341–1354

    Article  Google Scholar 

  • Devictor V, Julliard R, Couvet D, Jiguet F (2008) Birds are tracking climate warming, but not fast enough. P R Soc Biol Sci 275(1652):2743–2748

    Article  Google Scholar 

  • Diacon-Bolli J, Dalang T, Holderegger R, Bürgi M (2012) Heterogeneity fosters biodiversity: linking history and ecology of dry calcareous grasslands. Basic Appl Ecol 13:641–653

    Article  Google Scholar 

  • Douglas MM (1986) The lives of butterflies. University of Michigan Press, Ann Arbor

    Google Scholar 

  • Dover JW (1996) Factors affecting the distribution of satyrid butterflies on arable land. J Appl Ecol 33:723–734

    Article  Google Scholar 

  • Dover J, Sparks T (2000) A review of the ecology of butterflies in British hedgerows. J Environ Manag 60:51–63

    Article  Google Scholar 

  • Dover JW, Sparks TH, Greatorex-Davis JN (1997) The importance of shelter for butterflies in open landscapes. J Insect Conserv 1:89–97

    Article  Google Scholar 

  • Ekroos J, Heliölä J, Kuussaari M (2010) Homogenization of lepidopteran communities in intensively cultivated agricultural landscapes. J Appl Ecol 47:459–467

    Article  Google Scholar 

  • Erkinaro E, Heikura K, Lindgren E, Pulliainen E, Sulkava S (1982) Occurrence and spread of the wild boar (Sus scrofa) in eastern Fennoscandia. Memo Soc Fauna Flora Fennica 582:39–47

    Google Scholar 

  • Fernandez-Llario P (2004) Environmental correlates of nest site selection by wild boar Sus scrofa. Acta Theriol 49(3):383–392

    Article  Google Scholar 

  • Focardi S, Capizzi D, Monetti D (2000) Competition for acorns among wild boar (Sus scrofa) and small mammals in a Mediterranean woodland. J Zool 250:329–334

    Article  Google Scholar 

  • Franzén M, Ranius T (2004) Occurrence patterns of butterflies (Rhopalocera) in semi-natural pastures in southeastern Sweden. J Nat Conserv 12:121–135

    Article  Google Scholar 

  • Gallo Orsi U, Sicuro B, Durio P, Canalis L, Mazzoni G, Serzotti E, Chiariglione D (1995) Where and when: the ecological parameters affecting wild boars choice while rooting in grasslands in an alpine valley. IBEX J Mount Ecol 3:160–164

    Google Scholar 

  • Genov P (1981) Food composition of wild boar in north-eastern and western Poland. Acta Theriol 26:185–205

    Article  Google Scholar 

  • Gómez JM, González-Megías A (2007) Long-term effects of ungulates on phytophagous insects. Ecol Entomol 32:229–234

    Google Scholar 

  • Groot-Bruinderink GWTA, Hazebroek E (1996) Wild boar (Sus scrofa scrofa L.) rooting and forest regeneration on podzolic soils in the Netherlands. For Ecol Manage 88(1–2):71–80

    Article  Google Scholar 

  • Hawlena D, Bouskila A (2006) Land management practices for combating desertification cause species replacement of desert lizards. J Appl Ecol 43(4):701–709

    Article  Google Scholar 

  • Hayes L, Mann DJ, Monastyrskii AL, Lewis OT (2009) Rapid assessments of tropical dung beetle and butterfly assemblages: contrasting trends along a forest disturbance gradient. Insect Conserv Divers 2:194–203

    Article  Google Scholar 

  • Hone J (1988) Feral pig rooting in a mountain forest and woodland: distribution, abundance and relationship with environmental variables. Aust J Ecol 13:393–400

    Article  Google Scholar 

  • Hone J (1995) Spatial and temporal aspects of vertebrate pest damage with emphasis on feral pigs. J Appl Ecol 32:311–319

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Howe TD, Bratton SP (1976) Winter rooting activity of the European wild boar in the Great Smoky Mountains National Park. Castanea 41:256–264

    Google Scholar 

  • Howe TD, Singer FJ, Ackerman BB (1981) Forage relationships of European wild boar invading northern hardwood forest. J Wildl Manage 45:748–754

    Article  Google Scholar 

  • Kerr JT, Sugar A, Packer L (2000) Indicator Taxa, Rapid Biodiversity Assessment, and nestedness in a endangered ecosystem. Conserv Biol 14:1726–1734

    Article  Google Scholar 

  • Kitahara M, Sei K, Fujii K (2000) Patterns in the structure of grassland butterfly communities along a gradient of human disturbance: further analysis based on the generalist/specialist concept. Popul Ecol 42:135–144

    Article  Google Scholar 

  • Kotze J, Brandmayr P, Casale A, Dauffy-Richard E, Dekoninck W, Koivula M, Lovei G, Mossakowski D, Noordijk J, Paarmann W, Pizzoloto R, Saska P, Schwerk A, Serrano J, Szyszko J, Taboada A, Turin H, Venn S, Vermeulen R, Zetto Brandmayr T (2011) Forty years of carabid beetle research in Europe—from taxonomy, biology, ecology and population studies to bioindication, habitat assessment and conservation. ZooKeys 100:55–148

    Article  PubMed  Google Scholar 

  • Kurz JC, Marchinton RL (1972) Radiotelemetry studies of feral hogs in South Carolina. J Wildl Manage 36:1240–1248

    Article  Google Scholar 

  • Kuussaari M, Heliola J, Luoto M, Pőyry J (2007) Determinants of local species richness of diurnal Lepidoptera in boreal agricultural landscapes. Agr Ecosyst Environ 122:366–376

    Article  Google Scholar 

  • Larson G, Albarellad U, Dobneyb K, Rowley-Conwyb P, Schiblerf J, Tressetg A, Vigneg JD, Edwardsh CJ, Schlumbaumf A, Dinui A, Balaçsescuj A, Dolmank G, Tagliacozzol A, Manaseryanm N, Miraclen P, Van Wijngaarden-Bakkero L, Massetip M, Bradleyh DG, Cooperk A (2007) Ancient DNA, pig domestication, and the spread of the Neolithic into Europe. PNAS 104:15276–15281

    Article  PubMed  PubMed Central  Google Scholar 

  • Littlewood NA (2008) Grazing impacts on moth diversity and abundance on a Scottish upland estate. Insect Conserv Divers 1:151–160

    Article  Google Scholar 

  • Long JL (2003) Introduced mammals of the world: their history distribution and influence. CSIRO, Collingwood

    Google Scholar 

  • Mackin R (1970) Dynamics of damage by wild boar to different agricultural crops. Acta Theriol 27:447–458

    Article  Google Scholar 

  • Maselli V, Rippa D, Russo G, Ligrone R, Soppelsa O, D’Aniello B, Raia P, Fulgione D (2014) Wild boars’ social structure in the mediterranean habitat. Ital J Zoo 81(4):610–617

    Article  Google Scholar 

  • Maselli V, Rippa D, De Luca A, Larson G, Wilkens B, Linderholm A, Masseti M, Fulgione D (2016) Southern Italian wild boar population, hotspot of genetic diversity. Hystrix Ital J Mammal

  • Massei G, Genov PV (1995) Preliminary analysis of factors influencing habitat-use by the wild boar. Ibex J Mount Ecol 3:168–170

    Google Scholar 

  • Massei G, Genov PV (2004) The environmental impact of wild boar. Galemyis 16:135–145

    Google Scholar 

  • Meriggi A, Sacchi O (1992) Factors affecting damage by wild boars to cereal fields in northern Italy. Ongulés/Ungulates 91:439–441. S.F.E.P.M.-I.R.G.M, Toulouse

  • Meriggi A, Sacchi O (2001) Habitat requirements of wild boars in the northern Apennines (N Italy): a multi-level approach. Ital J Zoo 68(1):47–55

    Article  Google Scholar 

  • Moranz RA, Debinski DM, McGranahan DA, Engle DM, Miller JR (2012) Untangling the effects of fire, grazing, and land-use legacies on grassland butterfly communities. Biodiv Conserv 21:2719–2746

    Article  Google Scholar 

  • New T, Pyle R, Thomas J, Hammond P (1995) Butterfly conservation management. Ann Rev Entomol 40:57–83

    CAS  Article  Google Scholar 

  • O’Brien PH (1987) Socio-economic and biological impact of feral pig in New South Wales: an overview and alternative management plan. Rangel J 9:96–101

    Article  Google Scholar 

  • Öckinger E, Smith HG (2006) Landscape composition and habitat area affects butterfly species richness in semi-natural grasslands. Oecologia 149:526–534

    Article  PubMed  Google Scholar 

  • Öckinger E, Schweiger O, Crist TO, Debinski DM, Krauss J, Kuussaari M et al (2010) Life-history traits predict species responses to habitat area and isolation: a cross-continental synthesis. Ecol Lett 13:969–979

    PubMed  Google Scholar 

  • Onipchenko VG, Golikov KA (1996) Microscale revegetation of alpine lichen heath after wild boar digging: fifteen years of observation on permanent plots. Oecol Mont 5(1):35–39

    Google Scholar 

  • Palese AM, Pasquale V, Celano G, Figliuolo G, Masi S, Xiloyannis C (2009) Irrigation of olive groves in Southern Italy with treated municipal wastewater: effects on microbiological quality of soil and fruits. Agr Ecosyst Environ 129(1):43–51

    Article  Google Scholar 

  • Palese AM, Celano G, Xiloyannis C (2012) Esigenze minerali e tecniche di concimazione. In Accademia Nazionale dell'Olivo e dell'Olio (ed) Collana Divulgativa dell’Accademia, vol 10. Spoleto

  • PAST (2002) Data analysis package, version 0 × 94. Æyvindm Hammer, DAT Harper, Oslo

    Google Scholar 

  • Pe’er G, Settele J (2008) Butterflies in and for conservation: trends and prospects. Isr J Ecol Evol 54:7–17

    Article  Google Scholar 

  • Pe’er G, van Maanen C, Turbé A, Matsinos YG, Kark S (2011) Butterfly diversity at the ecotone between agricultural and semi-natural habitats across a climatic gradient. Divers Distrib 17:1186–1197

    Article  Google Scholar 

  • Pey B, Nahmani J, Auclerc A, Capowiez Y, Cluzeau D, Cortet J, Decaëns T, Deharveng L, Dubs F, Joimel S, Briard C, Grumiaux F, Laporte M, Pasquet A, Pelosi C, Pernin C, Ponge J, Salmon S, Santorufo L, Hedde M (2014) Current use of and future needs for soil invertebrate functional traits in community ecology. Basic Appl Ecol 15:94–206

    Article  Google Scholar 

  • Pizzolotto R, Brandmayr P (2014) IBP’: a new index to estimate biogeographical peculiarity. ISRN Ecol 2014:1–9

    Article  Google Scholar 

  • Pollard E, Yates TJ (1993) Monitoring butterflies for ecology and conservation. Chapman and Hall, London

    Google Scholar 

  • Polus E, Vandewoestijne S, Choutt J, Baguette M (2007) Tracking the effects of one century of habitat loss and fragmentation on calcareous grassland butterfly communities. Biodiv Conserv 16:3423–3436

    Article  Google Scholar 

  • Prola G, Prola C (1990) Libro rosso delle farfalle italiane (ed. by Fondo Mondiale per Natura), vol 13. WWF Quaderni

  • Rundlof M, Bengtsson J, Smith H (2008) Local and landscape effects of organic farming on butterfly species richness and abundance. J Appl Ecol 45:813–820

    Article  Google Scholar 

  • Sáez-Royuela C, Tellería JL (1986) The increased population of wild boar (Sus scrofa L.) in Europe. Mamm Rev 16:97–101

    Article  Google Scholar 

  • Scalercio S, Iannotta N, Brandmayr P (2007) The role of semi-natural and abandoned vegetation patches in sustaining lepidopteran diversity in an organic olive orchard. B Insectol 60:13–22

    Google Scholar 

  • Scalercio S, Brandmayr P, Iannotta N, Petacchi R, Bottaccio L (2012) Correlations between landscape attributes and ecological traits of Lepidoptera communities in olive groves. Eur J Entomol 109:207–216

    Article  Google Scholar 

  • Scandurra A, Magliozzi L, Aria M, D’Aniello B (2014) Short term effects of fire on Papillionoida (Lepidoptera) communities: a pilot study in Mediterranean maquis shrubland. Ital J Zool 81(4):599–609

    Article  Google Scholar 

  • Schley L, Roper J (2003) Diet of wild boar Sus scrofa in Western Europe, with particular reference to consumption of agricultural crops. Mamm Rev 33:43–56

    Article  Google Scholar 

  • Singer FJ, Swank WT, Clebsh EEC (1984) Effects of wild pig rooting in a deciduous forest. J Wildl Manage 48:464–473

    CAS  Article  Google Scholar 

  • Sisk TD, Launer AE, Switky KR, Ehrlich PR (1994) Identifying extinction threats: global analyses of the distribution and the expansion of the human enterprise. Bioscience 44:592–604

    Article  Google Scholar 

  • Smith LM, Cherry R (2014) Effects of management techniques on grassland butterfly species composition and community structure. Am Midl Nat 172:227–235

    Article  Google Scholar 

  • Stefanescu C, Herrando S, Páramo F (2004) Butterfly species richness in the north-west Mediterranean Basin: the role of natural and human-induced factors. J Biogeogr 31:905–915

    Article  Google Scholar 

  • Stefanescu C, Carnicer J, Peňuelas J (2011) Determinants of species richness in generalist and specialists Mediterranean butterflies: the negative synergistic forces of climate and habitat change. Ecography 34:353–363

    Article  Google Scholar 

  • Steffan-Dewenter I, Tscharntke T (2000) Butterfly community structure in fragmented habitats. Ecol Lett 3:449–456

    Article  Google Scholar 

  • Swengel AB (1996) Effects of fire and hay management on abundance of prairie butterflies. Biol Conserv 76:73–85

    Article  Google Scholar 

  • Swengel AB (1998) Effects of management on butterfly abundance in tallgrass prairie and pine barrens. Biol Conserv 83(1):77–89

    Article  Google Scholar 

  • Taron DJ (1997) Insects. In: Packard S, Matel CF (eds) The tallgrass restoration handbook: for prairies, savannas, and woodlands. Island Press, Washington

    Google Scholar 

  • Thomas JA (2005) Monitoring change in the abundance and distribution of insects using butterflies and other indicator groups. Phil Trans Roy Soc Lond B Biol Sci 360:339–357

    CAS  Article  Google Scholar 

  • Thomas JA, Telfer MG, Roy DB, Preston CD, Greenwood JJD, Asher J, Fox R, Clarke RT, Lawton JH (2004) Comparative losses of British butterflies, birds and plants and the global extinction crisis. Science 303:1879–1881

    CAS  Article  PubMed  Google Scholar 

  • Tscharntke T, Klein AM, Kruess A, Steffan-Dewenter I, Thies C (2005) Landscape perspectives on agricultural intensification and biodiversity—ecosystem service management. Ecol Lett 8:857–874

    Article  Google Scholar 

  • Van Noordwijk CGE, Flierman DE, Remke E, WallisDeVries MF, Berg MP (2012) Impact of grazing management on hibernating caterpillars of the butterfly Melitaea cinxia in calcareous grasslands. J Insect Conserv 16:909–920

    Article  Google Scholar 

  • van Swaay CAM, Warren M, Loïs G (2006) Biotope use and trends of European butterflies. J Insect Conserv 10:189–209

    Article  Google Scholar 

  • van Swaay C, Cuttelod A, Collins S, Maes D, Lopez Munguira M, Šašić M, Settele J, Verovnik R, Verstrael T, Warren M, Wiemers M, Wynhof I (2010) European Red list of butterflies. Luxembourg Publications Office of the European Union, Luxembourg

    Google Scholar 

  • Vassnat J (1996) Evolution of wild boar populations and damage to crops in France between 1978 and 1993. In: Proceeding of Schwarzwild symposium, Sopron, Ungarn, pp 131–141

  • Verdasca MJ, Leitão AS, Santana J, Porto M, Dias S, Beja P (2012) Forest fuel management as a conservation tool for early successional species under agricultural abandonment: the case of Mediterranean butterflies. Biol Conserv 146:14–23

    Article  Google Scholar 

  • Warren MS, Hill JK, Thomas JA (2001) Rapid responses of British butterflies to opposing forces of climate and habitat change. Nature 414:65–69

    CAS  Article  PubMed  Google Scholar 

  • Welander J (1995) Are wild boar a future threat to the Swedish flora? Ibex J Mount Ecol 3:165–167

    Google Scholar 

  • 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 

  • Wood GW, Roark DN (1980) Food habits of feral hogs in coastal South Carolina. J Wildl Manage 44:506–511

    Article  Google Scholar 

  • Wright DH, Patterson DD, Mikkelson GM, Cutler A, Atmar W (1998) A comparative analysis of nested subset patterns of species composition. Oecologia 113:1–20

    Article  Google Scholar 

  • Zivin J, Hueth BM, Zilberman D (2000) Managing a multiple-use resource: the case of feral pig management in California rangeland. J Environ Econ Manag 39:189–204

    Article  Google Scholar 

Download references

Acknowledgments

We are grateful to Mrs. Giuseppe Russo and Giovanni Pepe, for their perfect hospitality. We thank all of the property owners for tolerating our butterfly transects in their olive groves and all of the people who supported us in field during the research with their logistical support. Thanks also to the University of Naples for financial support and the National Park of “Cilento, Vallo di Diano and Alburni” for giving permission for the fieldwork.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Biagio D’Aniello.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Scandurra, A., Magliozzi, L., Fulgione, D. et al. Lepidoptera Papilionoidea communities as a sentinel of biodiversity threat: the case of wild boar rooting in a Mediterranean habitat. J Insect Conserv 20, 353–362 (2016). https://doi.org/10.1007/s10841-016-9863-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10841-016-9863-0

Keywords

  • Conservation
  • Diversity
  • Lepidoptera
  • Olive grove
  • Wild boar