Abstract
The wild pig (Sus scrofa) is an invasive species that negatively impacts new areas into which it is introduced. In this study, we evaluated the effects of wild pig presence on the estimated occupancy and detection probabilities of native mammals in the Brazilian Atlantic Forest. We used camera traps at 100 different points for 8 days (800 trap-days) to collect data and two-species conditional occupancy models to estimate the probability of occupancy (ψ) and the probability of detection (p) of mammal species. We detected a total of 23 native mammal species and two non-native mammal species [wild pig and European hare (Lepus europaeus)] and generated 21 models to evaluate the effects of wild pig occupancy on the European hare and the following 13 native mammals: Cerdocyon thous, Pseudalopex gymnocercus, Hydrochoerus hydrochaeris, Mazama americana, Mazama gouazoubira, Mazama nana, Dasyprocta aguti, Dasypus novemcinctus, Leopardus wiedii, Puma yagouaroundi, Didelphis albiventris, Conepatus chinga, and Procyon cancrivorus. Overall, the presence of wild pig had a range of negative effects on the occupancy and detection of the other mammals, which were less likely to occupy areas that were occupied by wild pig. In addition, we observed lower occurrence and richness of native mammal species in sampling points where wild pig were present compared with locations where wild pig were not present. These results highlight the importance of wild pig management and control for the conservation of native mammals in the Atlantic Forest, a region that is already threatened by a high degree of fragmentation.
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs10530-019-02068-9/MediaObjects/10530_2019_2068_Fig1_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs10530-019-02068-9/MediaObjects/10530_2019_2068_Fig2_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs10530-019-02068-9/MediaObjects/10530_2019_2068_Fig3_HTML.png)
Similar content being viewed by others
References
Ballari SA, Barrios-García MN (2014) A review of wild boar Sus scrofa diet and factors affecting food selection in native and introduced ranges. Mammal Rev 44:124–134
Barrios-García MN, Ballari SA (2012) Impact of wild boar (Sus scrofa) in its introduced and native range: a review. Biol Invasions 14:2283–2300
Barrios-García MN, Classen AT, Simberloff D (2014) Disparate responses of above-and belowground properties to soil disturbance by an invasive mammal. Ecosphere 5(4):1–13
Bellard C, Genovesi P, Jeschke JM (2016) Global patterns in threats to vertebrates by biological invasions. Proc R Soc 283(1823):20152454
Bianchi RDC, Rosa AF, Gatti A, Mendes SL (2011) Diet of margay, Leopardus wiedii, and jaguarundi, Puma yagouaroundi (Carnivora: Felidae) in Atlantic rainforest, Brazil. Zoologia 28(1):127–132
Branch LC (1995) Observations of predation by pumas and Geoffroy’s cats on the plains vizcacha in semi-arid scrub of central Argentina. Mammalia 59:152–156
Branch LC, Pessino M, Villarreal D (1996) Response of pumas to a population decline of the plains vizcacha. J Mammal 77:1132–1140
Brasil (2008) Plano de manejo da Estação Ecológica Aracuri-Esmeralda. Instituto Chico Mendes de Conservação da Biodiversidade, Brasília, Brazil
Burnham KP, Anderson DR (2002) Model selection and multi-model inference. A practical information-theoretic approach, 2nd edn. Springer, New York
Caruso N, Valenzuela AE, Burdett CL, Vidal EML, Birochio D, Casanave EB (2018) Summer habitat use and activity patterns of wild boar Sus scrofa in rangelands of central Argentina. PLoS ONE 13(10):e0206513
Cervo IB (2017) Dieta de Sus scrofa e suas implicações na agropecuária e na biodiversidade no Brasil. M.S.c, dissertation, Universidade Federal do Rio Grande do Sul, Porto Alegre
Chimera C, Coleman MC, Parkes JP (1995) Diet of feral goats and feral pigs on Auckland Island, New Zealand. N Z J Ecol 19:203–207
Choquenot D, McIlroy J, Korn T (1996) Managing vertebrate pests: feral pigs. Australian Government Publishing Service, Bureau of Resource Sciences, Canberra
Deberdt AJ, Scherer SB (2007) O javali asselvajado: ocorrência e manejo da espécie no Brasil. Nat Conserv 5:31–44
Desbiez ALJ, Santos SA, Keuroghlian A, Bodmer RE (2009) Niche partitioning among white-lipped peccaries (Tayassu pecari), collared peccaries (Pecari tajacu), and feral pigs (Sus scrofa). J Mammal 90:119–128
Focardi S, Capizzi D, Monetti D (2000) Competition for acorns among wild boar (Sus scrofa) and small mammals in a Mediterranean woodland. J Zool (Lond) 250:329–334
Fonseca GA (1994) Livro vermelho dos mamíferos brasileiros ameaçados de extinção. Fundação Biodiversitas, Belo Horizonte
Forsyth DM, Allen RB, Allen RK, Affeld K, MacKenzie DI (2016) Soil phosphorus predicts feral pig (Sus scrofa) occupancy, detection probability and feeding activity in a temperate montane rainforest. Wildl Res 43(4):277–287
Frehse FA, Braga RR, Nocera GA, Vitule JRS (2016) Non-native species and invasion biology in a megadiverse country: scientometric analysis and ecological interactions in Brazil. Biol Invasions 18:3713–3725
Galetti M, Camargo H, Siqueira T, Keuroghlian A, Donatti CI, Jorge MLSP, Pedrosa F, Kanda CZ, Ribeiro MC (2015) Diet overlap and foraging activity between feral pigs and native peccaries in the Pantanal. PLoS ONE 10(11):e0141459
Gantchoff MG, Belant JL (2015) Anthropogenic and environmental effects on invasive mammal distribution in northern Patagonia, Argentina. Mammal Biol Zeitschr Säuget 80(1):54–58
Giménez-Anaya A, Herrero J, Rosell C, Couto S, García-Serrano A (2008) Food habits of wild boar (Sus scrofa) in a Mediterranean coastal wetland. Wetlands 28:197–203
Graitson E, Barbraud C, Bonnet X (2018) Catastrophic impact of wild boars: insufficient hunting pressure pushes snakes to the brink. Anim Conserv. https://doi.org/10.1111/acv.12447
Graves H (1984) Behavior and ecology of wild and feral swine (Sus scrofa). J Anim Sci 58:482
Grossi SF, Lui JF, Garcia JE, Meirelles VF (2006) Genetic diversity in wild pig (Sus scrofa scrofa) and domestic pig (Sus scrofa domestica) and their hybrids based on polymorphism of a fragment of the D loop region in the mitochondrial DNA. Genet Mol Res 5(4):564–568
Hegel CGZ, Marini MÂ (2013) Impact of the wild boar, Sus scrofa, on a fragment of Brazilian Atlantic Forest. Neotrop Biol Conserv 8:17–24
Hegel CGZ, Marini MÂ (2018) Large felids as predators of wild boar in the Atlantic Forest: reconciling Verdade, and Rosa et al. Anim Conserv 21:363–364
Hegel CGZ, Santos LR, Pichorim M, Marini MÂ (2019) Wild pig (Sus scrofa L.) occupancy patterns in the Brazilian Atlantic forest. Biota Neotrop 19(4):e20180719
Heise-Pavlov PM, Heise-Pavlov SR, Nelson JE (2009) Sus scrofa: population structure, reproduction and condition in tropical north-eastern Australia. Acta Silv Lign Hung 5:179–188
Herrero J, García-Serrano A, Couto S, Ortuño VM, García-González R (2006) Diet of wild boar Sus scrofa L. and crop damage in an intensive agroecosystem. Eur J Wildl Res 52:245–250
IBAMA (2013) Instrução Normativa Ibama Nº 03 de 31 de janeiro de 2013 do Instituto Brasileiro do Meio Ambiente e dos Recursos Renováveis (IBAMA). Brasília: Ministério do Meio Ambiente (MMA)
IBAMA (2019) Instrução Normativa Ibama Nº 12 de 25 de março de 2019 do Instituto Brasileiro do Meio Ambiente e dos Recursos Renováveis (IBAMA). Brasília: Ministério do Meio Ambiente (MMA)
Ilse LM, Hellgren EC (1995) Resource partitioning in sympatric populations of collared peccaries and feral hogs in Southern Texas. J Mammal 76(3):784–799
Irizar I, Laskurain NA, Herrero J (2004) Wild boar frugivory in the Atlantic Basque Country. Galemys 16:125–133
IUCN - International Union for Conservation of Nature (2017) The IUCN red list of threatened species. http://www.iucnredlist.org/search/details. Accessed date: 09 Nov 2017
Jaksic FM, Agustín Iriarte J, Jiménez JE, Martínez DR (2002) Invaders without frontiers: cross-border invasions of exotic mammals. Biol Invasions 4:157–173
Jedrzejewski W, Jedrzejewska B, Okarma H, Ruprecht AL (1992) Wolf predation and snow cover as mortality factors in the ungulate community of the Białowieza National Park, Poland. Oecologia 90:27–36
Keiter DA, Mayer JJ, Beasley JC (2016) What is in a “common” name? A call for consistent terminology for nonnative Sus scrofa. Wildl Soc Bull 40(2):384–387
Lavers C (2011) Why elephants have big ears: understanding patterns of life on earth. Macmillan. ISBN:9781429976695
Lazenby BT, Dickman CR (2013) Patterns of detection and capture are associated with cohabiting predators and prey. PLoS ONE 8:e59846
Leger EA, Espeland EK (2010) Coevolution between native and invasive plant competitors: implications for invasive species management. Evol Appl 3:169–178
Long JL (2003) Introduced mammals of the world: their history distribution and influence. CSIRO, Collingwood
MacKenzie DI, Royle JA (2005) Designing occupancy studies: general advice and allocating survey effort. J Appl Ecol 42:1105–1114
MacKenzie DI, Bailey LL, Nichols J (2004) Investigating species co-occurrence patterns when species are detected imperfectly. J Anim Ecol 73:546–555
MacKenzie DI, Nichols JD, Royle JA, Pollock KH, Bailey LL, Hines JE (2006) Occupancy estimation and modeling: inferring patterns and dynamics of species occurrence. Academic Press, Burlington
Marques AAB, Fontana CS, Vélez E, Bencke GA, Schneider M, Reis RE (2002) Lista de referência da fauna ameaçada de extinção no Rio Grande do Sul. Decreto no 41.672, de 11 junho de 2002. Porto Alegre: FZB/MCT–PUCRS/PANGEA, 52p
Marsan A, Mattioli S (2013) Il Cinghiale (in Italian). Il Piviere (collana Fauna selvatica. Biologia e gestione). ISBN 978-88-96348-178
Massei G, Genov PV (2004) The environmental impact of wild boar. Galemys 16(Special edition):135–145
Mattioli L, Apollonio M, Lovari C, Siemoni N, Crudele G (1995) Wild boar as the main prey of wolf in an area of Northern Apennines (Italy), Ibex. J Mt Ecol 3:212
Means DB, Travis J (2007) Declines in ravine-inhabiting dusky salamanders of the southeastern US Coastal Plain. Southeast Nat 6(1):83–97
Melletti M, Meijaard E (2017) Ecology, conservation and management of wild pigs and peccaries. Cambridge University Press, Cambridge
Mendina Filho LH, Wallau MO, Dos Reis TX (2015) O Javali no Pampa: contexto, biologia e manejo. Pallotti, Santana do Livramento. 87p
Myers N, Mittermeier RA, Mittermeier CG, Fonseca GAB, Jennifer K (2000) Biodiversity hotspots for conservation priorities. Nature 403:853–858
Nagy-Reis MB, Nichols JD, Chiarello AG, Ribeiro MC, Setz EZ (2017) Landscape use and co-occurrence patterns of Neotropical spotted cats. PLoS ONE 12(1):e0168441
Nores C, Llaneza L, Álvarez MA (2008) Wild boar Sus scrofa mortality by hunting and wolf Canis lupus predation: an example in northern Spain. Wildl Biol 14:44–51
Novack AJ, Main MB, Sunquist ME, Labisky RF (2005) Foraging ecology of jaguar (Panthera onca) and puma (Puma concolor) in hunted and non-hunted sites within the Maya Biosphere Reserve, Guatemala. J Zool 267:167–178
Novaro AJ, Funes MC, Walker RS (2000) Ecological extinction of native prey of a carnivore assemblage in Argentine Patagonia. Biol Conserv 92:25–33
O’Brien PP, Vander Wal E, Koen EL, Brown C, Guy J, van Beest FM, Brook RK (2019) Understanding habitat co-occurrence and the potential for competition between native mammals and invasive wild pigs at the northern edge of their range. Can J Zool 1:21. https://doi.org/10.1139/cjz-2018-0156
O’Connell AF Jr, Talancy NW, Bailey LL, Sauer JR, Cook R, Gilbert AT (2006) Estimating site occupancy and detection probability parameters for meso-and large mammals in a coastal ecosystem. J Wildl Manag 70:1625–1633
Oliveira-Santos LGR, Dorazio RM, Tomas WM, Mourão G (2011) No evidence of interference competition among the invasive feral pig and two native peccary species in a Neotropical wetland. J Trop Ecol 27:557–561
Osugi S, Trentin BE, Koike S (2019) Impact of wild boars on the feeding behaviors of smaller frugivorous mammals. Mamm Biol. https://doi.org/10.1016/j.mambio.2019.03.013
Pedrosa F, Salerno R, Padilha FVB, Galetti M (2015) Current distribution of invasive feral pigs in Brazil: economic impacts and ecological uncertainty. Nat Conserv 13:84–87
Pérez Carusi LC, Beade MS, Miñarro F, Vila AR, Giménez-Dixon M, Bilenca DN (2009) Relaciones espaciales y numéricas entre venados de las pampas (Ozotoceros bezoarticus celer) y chanchos cimarrones (Sus scrofa) en el Refugio de Vida Silvestre Bahía Samborombón, Argentina. Ecol Austral 19:63–71
Pessino MEM, Sarasola JH, Wander C, Besoky N (2001) Respuesta a largo plazo del puma (Puma concolor) a una declinación poblacional de la vizcacha (Lagostomus maximus) en el desierto del Monte, Argentina. Ecol Austral 11:61–67
Peters FB, Roth PRDO, Christoff AU (2011) Feeding habits of Molina’s hog-nosed skunk, Conepatus chinga (Carnivora: Mephitidae) in the extreme south of Brazil. Zoologia (Curitiba) 28(2):193–198
Quintela FM, Santos MB, Oliveira SV, Costa RC, Christoff AU (2010) Wild boars and feral pigs (Suidae, Sus scrofa) in the Restinga of Rio Grande, RS, Brazil: ecosystems of occurrence and preliminary data on environmental impacts. Neotrop Biol Conserv 5:172–178
R Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/
Reis NR, Peracchi AL, Pedro WA, Lima IP (2006) Mamíferos do Brasil. Nélio R. dos Reis, Londrina, Brazil. 437p
Richmond OM, Hines JE, Beissinger SR (2010) Two-species occupancy models: a new parameterization applied to co-occurrence of secretive rails. Ecol Appl 20:2036–2046
Rocha VJ, Aguiar LM, Silva-Pereira JE, Moro-Rios RF, Passos FC (2008) Feeding habits of the crab-eating fox, Cerdocyon thous (Carnivora: Canidae), in a mosaic area with native and exotic vegetation in Southern Brazil. Rev Bras Zool 25(4):594–600
Rosa CA, Puertas F, Galetti M (2016) The feral pig as prey for jaguars: a reply to the ‘letter from the conservation front line’ by Verdade et al. Anim Conserv 20:111–112
Rosell C, Fernández-Llario P, Herrero J (2001) El jabalí (Sus scrofa Linnaeus, 1758). Galemys 13:1–25
Sales LP, Ribeiro BR, Hayward MW, Paglia A, Passamani M, Loyola R (2017) Niche conservatism and the invasive potential of the wild boar. J Anim Ecol 86(5):1214–1223
Salvador CH, Tortatto MA, Miozzo R, Copini AC (2013) Análise de diferentes tipos de cevas no monitoramento de populações selvagens de javali (Sus scrofa) e prejuízos ocasionados em plantação de milho no interior do município de Caçador. Ignis 2(1):71–83
Sicuro FL, Oliveira LFB (2002) Coexistence of peccaries and feral hogs in the Brazilian Pantanal wetland: an ecomorphological view. J Mammal 83:207–217
Silva F (1994) Mamíferos silvestres do Rio Grande do Sul. Fundação Zoobotânica do Rio Grande do Sul, Porto Alegre
Simberloff D, Martin J-L, Genovesi P, Maris V, Wardle DA, Aronson J, Courchamp F, Galil B, García-Berthou E, Pascal M, Pyšek P, Sousa R, Tabacchi E, Vilà M (2013) Impacts of biological invasions: what’s what and the way forward. Trends Ecol Evol 28:58–66
Singer FJ, Swank WT, Clebsch EEC (1984) Effects of wild pig rooting in a deciduous forest. J Wildl Manag 48:464–473
Skewes O, Moraga CA, Arriagada P, Rau JR (2012) El jabalí europeo (Sus scrofa): Un invasor biológico como presa reciente del puma (Puma concolor) en el sur de Chile. Rev Chil Hist Nat 85:227–232
Sweitzer RA, Van Vuren DH (2002) Rooting and foraging effects of wild pigs on tree regeneration and acorn survival in California’s oak woodland ecosystems. USDA Forest Service General Technical Reports 184, pp 219–231
Vanak AT, Gompper ME (2010) Interference competition at the landscape level: the effect of free-ranging dogs on a native mesocarnivore. J Appl Ecol 47:1225–1232
Verdade LM, Palomares F, Couto HTZ, Polizel JL (2015) Recent land-use changes and the expansion of an exotic potential prey: a possible redemption for Atlantic forest jaguars? Anim Conserv 19:209–211
Verdade LM, Palomares F, Couto HTZ, Polizel JL (2017) Land-use change and an exotic potential prey for the jaguar: a reply to da Rosa et al. Anim Conserv 21(2):89–90
Weckel M, Giuliano W, Silver S (2006) Jaguar (Panthera onca) feeding ecology: distribution of predator and prey through time and space. J Zool 270:25–30
West BC, Cooper AL, Armstrong JB (2009) Managing wild pigs: a technical guide. Hum Wildl Interact Monogr 1:1–55
White GC, Burnham KP (1999) Program MARK: survival estimation from populations of marked animals. Bird Study 46(Supplement):120–138
Wilcox JT, Van Vuren DH (2009) Wild pigs as predators in oak woodlands of California. J Mammal 90:114–118
Zapata-Ríos G, Branch LC (2016) Altered activity patterns and reduced abundance of native mammals in sites with feral dogs in the high Andes. Biol Conserv 193:9–16
Acknowledgements
We thank CAPES, CNPq, and FAP-DF for fellowships to the authors, and URI and UnB for logistical and financial support. MÂM was supported by a researcher fellowship from CNPq. ICMBio provided a license to conduct research at the ESEC Aracuri-Esmeralda reserve. We are also grateful to A. Gedoz, A, Faraon, and D.C. Rith for the support in the field, to J.R.S. Vitule, L.U. Hepp, R. Fornel, J.A.B. Monsalvo, and S.M.S. Róseo for their useful critiques of earlier manuscript drafts, and to the landowners who provided access to their properties.
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Hegel, C.G.Z., Santos, L.R., Marinho, J.R. et al. Is the wild pig the real “big bad wolf”? Negative effects of wild pig on Atlantic Forest mammals. Biol Invasions 21, 3561–3574 (2019). https://doi.org/10.1007/s10530-019-02068-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10530-019-02068-9