Abstract
Monitoring populations of elusive large carnivores like wolves (Canis lupus), which are often distributed at low density in widespread forested areas, is difficult or exceedingly expensive. Aiming to assess the power of two indirect monitoring methods, non-invasive genetic sampling and camera trapping, we designed a small-scale pilot study that was carried out from 2006 to 2008 in and around the Corno alle Scale Regional Park, Bologna, northern Italian Apennine. We collected 103 non-invasive samples (mainly scats) that were genotyped at 12 microsatellite loci and sexed using the ZFX gene. We identified 11 distinct wolf genotypes within the park and four wolf genotypes outside. Spatial locations and kinship analyses showed that the wolves belong to three different packs. The breeding pair of the ‘Park’ pack showed a complete turnover in the two sampling seasons. Two dogs, but no hybrids, were identified in the area. Up to five unbaited camera traps were activated (for 1,250 trapping-nights) close to recent wolf presence marks. We obtained 103 photos of wolves, documenting the reproduction events, the minimum number of adult and young wolves, and phenotype information each year. We obtained information on health conditions detecting probable sarcoptic mange in three individuals. Camera trapping also showed that the presence of wolves in a chase area during wild boar (Sus scrofa) hunting sessions was significantly higher in the nights just after a chase (P < 0.01, χ 2 test; P < 0.07¸ exact Fisher test). The data obtained from genetics and camera trapping were consistent with one other, and in part complementary. The total cost of the study (c. 28,000 €) was moderate, suggesting that this integrated approach can be successfully used to monitor the structure and dynamics of local wolf packs.
Similar content being viewed by others
References
Altobello G (1921) Mammiferi IV, Carnivori. In: Fauna d’Abruzzo e Molise. Campobasso, Italy, pp 38–45
Anderson TM, vonHoldt BM, Candille SI et al (2009) Molecular and evolutionary history of melanism in North American gray wolves. Science 323:1339–1343
Anwar SM, Musiani M, McDermid G, Marceau D (2009) How do human activities shape wolves’ behavior in the central Rocky Mountains region, Alberta, Canada? Proceedings of the 2009 Spring Simulation Multiconference. San Diego, California
Apollonio M, Mattioli L, Scandura M, Mauri L, Gazzola A, Avanzinelli E (2004) Wolves in the Casentinesi Forests: insights for wolf conservation in Italy from a protected area with a rich wild prey community. Biol Conserv 120:249–260
Barja I, De Miguel FJ, Barcena F (2004) The importance of crossroads in faecal marking behaviour of the wolves (Canis lupus). Naturwissenschaften 91:489–492
Berzi D, Groff G (2002) L’uso delle trappole fotografiche per indagini faunistiche sul lupo e su altri grandi carnivori: prime indicazioni sulla sperimentazione in Italia. In: Boscagli G, Vielmi L, De Curtis O (eds) Atti del convegno “Il lupo e i parchi”. Parco Nazionale delle Foreste Casentinesi, Italy, pp 154–160
Boitani L (2003) Wolf conservation and recovery. In: Mech LD, Boitani L (eds) Wolves behavior ecology and conservation. University of Chicago, Chicago, pp 317–340
Brainerd SM, Adrén M, Bangs EE et al (2008) The effect of breeder loss on wolves. J Wildl Manag 72:89–98
Breitenmoser U (1998) Large predators in the Alps: the fall and rise of men’s competitors. Biol Conserv 83:279–289
Brøseth H, Flagstad Ø, Wärdig C, Johansson M, Ellegren H (2010) Large-scale noninvasive genetic monitoring of wolverines using scats reveals density dependent adult survival. Biol Conserv 143:113–120
Caniglia R, Fabbri E, Greco C, Martelli D, Paladini G, Rigacci L, Randi E (2010a) Presenza e distribuzione del lupo (Canis lupus) in Provincia di Bologna. Risultati ottenuti mediante l’utilizzo integrato di diverse tecniche non-invasive. In: Caniglia R, Fabbri E, Greco C, Randi E (Eds.), Atti del convegno Ricerca scientifica e strategie per la conservazione del lupo (Canis lupus) in Italia. Quad Conserv Nat 33, Min. Ambiente—ISPRA, pp 129–169
Caniglia R, Fabbri E, Greco C, Randi E (2010b) Monitoraggio della presenza del lupo (Canis lupus) in Emilia-Romagna tramite campionamento genetico non-invasivo. In: Caniglia R, Fabbri E, Greco C, Randi E (eds) Atti del convegno Ricerca scientifica e strategie per la conservazione del lupo (Canis lupus) in Italia. Quad Conserv Nat 33, Min. Ambiente—ISPRA, pp 19–66
Caniglia R, Fabbri E, Greco C, Galaverni M, Randi E (2010c) Forensic DNA against wildlife poaching: Identification of a serial wolf killing in Italy. Forensic Sci Int Genet 4:334–338
Carbone C, Christie S, Conforti K et al (2001) The use of photographic rates to estimate densities of tigers and other cryptic mammals. Anim Conserv 4:75–79
Carr AP, Rodgers AR (1998) HRE: the home range extension for ArcView. Ontario Ministry of Natural Resources, Thunder Bay
Cercueil A, Bellemain E, Manel S (2002) Parente: computer program for parentage analysis. J Hered 93:458–459
Ciucci P, Boitani L (1998) Wolf and dog depredation on livestock in central Italy. Wildl Soc Bull 26:504–514
Ciucci P, Boitani L, Francisci F, Andreoli G (1997) Home range, activity and movements of a wolf pack in central Italy. J Zool 243:803–819
Ciucci P, Chapron G, Guberti V, Boitani L (2007) Estimation of mortality parameters from (biased) samples at death: are we getting the basics right in wildlife field studies? A response to Lovari et al. J Zool 273:125–127
Corsi F, Duprè E, Boitani L (1999) A large-scale model of wolf distribution in Italy for conservation planning. Conserv Biol 13:150–159
Cozza K, Fico R, Battistini ML, Rogers E (1996) The damage-conservation interface illustrated by predation on domestic livestock in central Italy. Biol Conserv 78:329–336
Cubaynes S, Pradel R, Choquet R et al (2010) Importance of accounting for detection heterogeneity when estimating abundance: the case of French wolves. Conserv Biol 24:621–626
Cutler TL, Swann DE (1999) Using remote photography in wildlife ecology: a review. Wildl Soc Bull 27:571–581
De Barba M, Waits LP, Genovesi P, Randi E, Chirichella R, Cetto E (2010) Comparing opportunistic and systematic sampling methods for non-invasive genetic monitoring of a small translocated brown bear population. J Appl Ecol 47:172–181
Fabbri E, Miquel C, Lucchini V et al (2007) From the Apennines to the Alps: colonization genetics of the naturally expanding Italian wolf (Canis lupus) population. Mol Ecol 16:1661–1671
Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164:1567–1587
Francisci F, Guberti V (1993) Recent trends of wolves in Italy as apparent from kill figures and specimens. In: Promberger C, Schroder W (eds) Wolves in Europe Status and perspectives. Munich Wildlife Society, Munich, Germany, pp 91–102
Francisco LV, Langston AA, Mellersh CS, Neal CL, Ostrander EA (1996) A class of highly polymorphic tetranucleotide repeats for canine genetic mapping. Mamm Genome 7:359–362
Fredholm M, Winterø AK (1995) Variation of short tandem repeats within and between species belonging to the Canidae family. Mamm Genome 6:11–18
Gazzola A, Capitani C, Mattioli L, Apollonio M (2008) Livestock damage and wolf presence. J Zool 274:261–269
Genovesi P (2002) Piano d’azione nazionale per la conservazione del Lupo (Canis lupus). Quad Conserv Nat 13. Ministero dell’Ambiente e della Tutela del Territorio—Istituto Nazionale per la Fauna Selvatica, Italy
Gervasi V, Ciucci P, Boulanger J, Posillico M, Sulli C, Focardi S, Randi E, Boitani L (2008) A preliminary estimate of the Apennine brown bear population size based on hair-snag sampling and multiple data source mark-recapture Huggins models. Ursus 19:105–121
Gese EM (2001) Monitoring of terrestrial carnivore populations. In: Gittleman JL, Funk SM, MacDonald DW, Wayne RK (eds) Carnivores Conservation. Cambridge University Press & The Zoological Society of London, UK, pp 372–396
Gompper ME, Kays RW, Ray JC, Lapoint SD, Bogan DA, Cryan JR (2006) A comparison of noninvasive techniques to survey carnivore communities in northeastern North America. Wildl Soc Bull 34:1142–1151
Harrison RL, Barr DJ, Dragoo JW (2002) A comparison of population survey techniques for swift foxes (Vulpes velox) in New Mexico. Am Midl Nat 148:320–337
Jędrzejewski W, Schmidt K, Jędrzejewska B, Theuerkauf J, Kowalczyk R, Zub K (2004) The process of a wolf pack splitting in Bialowieża Primeval Forest, Poland. Acta Theriol 49:275–280
Jędrzejewski W, Branicki W, Veit C et al (2005) Genetic diversity and relatedness within packs in an intensely hunted population of wolves Canis lupus. Acta Theriol 50:3–22
Kalinowski ST, Sawaya MA, Taper ML (2006) Individual identification and distribution of genotypic differences between individuals. J Wildl Manag 70:1148–1150
Karanth KU, Nichols JD (1998) Estimation of tiger densities in India using photographic captures and recaptures. Ecology 79:2852–2862
Karanth KU, Nichols JD, Kumar NS, Hines JE (2006) Assessing tiger population dynamics using photographic capture-recapture sampling. Ecology 87:2925–2937
Kernohan BJ, Gitzen RA, Millspaugh JJ (2001) Analysis of animal space use and movement. In: Millspaugh JJ, Marzluff JM (eds) Radio tracking and animal populations. Academic, San Diego, CA, pp 126–166
Kohn MH, Wayne RK (1997) Facts from faeces revisited. TREE 12:223–227
Kreeger TJ (2003) The internal wolf: physiology, pathology, and pharmacology. In: Mech LD, Boitani L (eds) Wolves behavior, ecology, and conservation. University of Chicago, Chicago, USA, pp 192–217
Kucera TE, Barrett RH (1993) The trailmaster camera system for detecting wildlife. Wildl Soc Bull 21:505–508
Larrucea ES, Brussard PF, Jaeger MM, Barrett RH (2007) Cameras, coyotes, and the assumption of equal detectability. J Wildl Manag 71:1682–1689
Lovari S, Sforzi A, Scala C, Fico R (2007) Mortality parameters of the wolf in Italy: does the wolf keep himself from the door? J Zool 272:117–124
Lucchini V, Fabbri E, Marucco F, Ricci S, Boitani L, Randi E (2002) Non-invasive molecular tracking of colonizing wolf (Canis lupus) packs in the western Italian Alps. Mol Ecol 11:857–868
Marucco F, Pletscher DH, Boitani L, Schwartz MK, Pilgrim KL, Lebreton JD (2009) Wolf survival and population trend using non-invasive capture-recapture techniques in the Western Alps. J Appl Ecol 46:1003–1010
Mech LD (1970) The wolf: the ecology and behavior of an endangered species. Natural History Press, Doubleday, New York, USA
Mech LD, Boitani L (2003) Wolf social ecology. In: Mech LD, Boitani L (eds) Wolves behavior ecology and conservation. University of Chicago, Chicago, USA, pp 1–34
Miller C, Joyce P, Waits L (2002) Assessing allelic dropout and genotype reliability using maximum likelihood. Genetics 160:357–366
Mills LS, Pilgrim KL, Schwartz MK, McKelvey K (2000a) Identifying lynx and other North American felids based on MtDNA analysis. Conserv Genet 1:285–288
Mills LS, Citta JJ, Lair KP, Schwartz MK, Tallmon DA (2000b) Estimating animal abundance using noninvasive DNA sampling: promise and pitfalls. Ecol Appl 10:283–294
Moruzzi TL, Fuller TK, DeGraaf RM, Brooks RT, Wenjun L (2002) Assessing remotely triggered cameras for surveying carnivore distribution. Wildl Soc Bull 30:380–386
Nilsson T (2003) Integrating effects of hunting policy, catastrophic events, and inbreeding depression, in PVA simulation: the Scandinavian wolf population as an example. Biol Conserv 115:227–239
Oliveira-Santos LGR, Zucco CA, Castro Antunes P, Crawshaw PG Jr (2009) Is it possible to individually identify mammals with no natural markings using camera-traps? A controlled case-study with lowland tapirs. Mamm Biol. doi:10.1016/j.mambio.2009.08.005
Ostrander EA, Sprague GF, Rine J (1993) Identification and characterization of dinucleotide repeat (CA)n markers for genetic mapping in dog. Genomics 16:207–213
Palomares F, Godoy A, Piriz A, O’Brien SJ, Johnson WE (2002) Faecal genetic analysis to determine the presence and distribution of elusive carnivores: design and feasibility for the Iberian lynx. Mol Ecol 11:2171–2182
Palumbo D, Galaverni M, Fabbri E, Caniglia R, Greco C, Sarno S, Randi E (2010) Monitoraggio del lupo (Canis lupus) nel Parco regionale del Corno alle Scale tramite foto-videotrappolaggio e genetica non invasiva: un nuovo modello di studio integrato. In: Caniglia R, Fabbri E, Greco C, Randi E (eds) Atti del convegno Ricerca scientifica e strategie per la conservazione del lupo (Canis lupus) in Italia. Quad Conserv Nat 33, Min. Ambiente—ISPRA, pp 171–196
Pereira A, Oliveira R, Alves PC, Schwartz MK, Luikart G (2009) Advancing ecological understandings through technological transformations in non-invasive genetics. Mol Ecol Resour 9:1279–1301
Peters RP, Mech LD (1975) Scent-Marking in Wolves. Am Sci 63:628–637
Peterson RO, Jacobs AM, Drummer TD, Mech LD, Smith DW (2002) Leadership behavior in relation to dominance and reproductive status in gray wolves, Canis lupus. Can J Zool 80:1405–1412
Queller DC, Goodnight KF (1989) Estimating relatedness using genetic markers. Evolution 43:258–275
Randi E (2005) Management of wild ungulate populations in Italy: captive-breeding, hybridisation and genetic consequences of translocation. Vet Res Commun 29:71–75
Randi E, Lucchini V (2002) Detecting rare introgression of domestic dog genes into wild wolf (Canis lupus) populations by Bayesian admixture analyses of microsatellite variation. Conserv Genet 3:29–43
Rosellini S, Osorio E, Ruiz-Gonzales A, Piñeiro A, Barja I (2008) Monitoring the small-scale distribution of sympatric European pine martens (Martes martes) and stone martens (Martes foina): a multievidence approach using faecal DNA analysis and camera-traps. Wildl Res 35:434–440
Santini A, Lucchini V, Fabbri E, Randi E (2007) Ageing and environmental factors affect PCR success in wolf (Canis lupus) excremental DNA samples. Mol Ecol Notes 7:955–961
Sarmento P, Cruz J, Monterroso P, Tarroso P, Ferreira C, Negrões N, Eira C (2009) Status survey of the critically endangered Iberian lynx Lynx pardinus in Portugal. Eur J Wildl Res 55:247–253
Schwartz MK, Luikart G, Waples RS (2007) Genetic monitoring as a promising tool for conservation and management. Trends Ecol Evol 22:25–33
Seaman DE, Millspaugh JJ, Kernohan BJ, Brundige GC, Raedeke KJ, Gitzen RA (1999) Effects of sample size on kernel home range estimates. J Wildl Manag 63:739–747
Seydack AH (1984) Application of a photo recording device in the census of larger rain forest mammals. S Afr J Wildl Res 14:10–14
Sidorovich VE, Stolyarov VP, Vorobei NN, Ivanova NV, Jedrzejewska B (2007) Litter size, sex ratio, and age structure of gray wolves, Canis lupus, in relation to population fluctuations in northern Belarus. Can J Zool 85:295–300
Solberg KH, Bellemain E, Drageset OM, Taberlet P, Swenson JE (2006) An evaluation of field and non-invasive genetic methods to estimate brown bear (Ursus arctos) population size. Biol Conserv 128:158–168
Spalton A (2002) Canidae in the Sultanate of Oman. Canid News 5:1. http://www.canids.org/canidnews/5/canids_in_oman.pdf. Accessed 23 Sep 2009
Taberlet P, Camarra JJ, Griffin S, Uhrès E, Hanotte O, Waits LP, Dubois-Paganon C, Burke T, Bouvet J (1997) Noninvasive genetic tracking of the endangered Pyrenean brown bear population. Mol Ecol 6:869–876
Valière N (2002) GIMLET: a computer program for analysing genetic individual identification data. Mol Ecol Notes 2:377–379
Van Schaik CO, Griffiths M (1996) Activity periods of Indonesian rain forest mammals. Biotropica 28:105–112
Verardi A, Lucchini V, Randi E (2006) Detecting introgressive hybridisation between free-ranging domestic dogs and wild wolves (Canis lupus) by admixture linkage disequilibrium analysis. Mol Ecol 15:2845–2855
Vilà C, Urios V, Castroviejo J (1994) Use of faeces for scent marking in Iberian wolves (Canis lupus). Can J Zool 72:374–377
Waits LP, Paetkau D (2005) Noninvasive genetic sampling tools for wildlife biologists: a review of applications and recommendations for accurate data collection. J Wildl Manag 4:1419–1433
Waits LP, Luikart G, Taberlet P (2001) Estimating the probability of identity among genotypes in natural populations: cautions and guidelines. Mol Ecol 10:249–256
Wang J, Santure AW (2009) Parentage and sibship inference from multi-locus genotype data under polygamy. Genetics 181:1579–1594
Worton BJ (1989) Kernel methods for estimating the utilization in home-ranges studies. Ecology 70:164–168
Acknowledgements
We would like to thank E. Centofanti, Natura Service, for providing all the camera trapping equipment; S. Cavicchi, University of Bologna, and A. Papeschi, University of Florence, for their advice in planning the eco-ethological test; S. Sarno (student at University of Bologna) for her collaboration in the field work; G. Pontrandolfo (University of Trieste) and J. Robinson (UCLA) for linguistic assistance. Genotyping at the Conservation Genetics Lab (ISPRA) was supported by the Italian Ministry of Environment (thanks to General Director of Nature Conservation, Dr. A. Cosentino), and by the Emilia-Romagna Region (thanks to Dr. M.L. Bargossi and Dr. M.L. Zanni).
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by C. Gortázar
Rights and permissions
About this article
Cite this article
Galaverni, M., Palumbo, D., Fabbri, E. et al. Monitoring wolves (Canis lupus) by non-invasive genetics and camera trapping: a small-scale pilot study. Eur J Wildl Res 58, 47–58 (2012). https://doi.org/10.1007/s10344-011-0539-5
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10344-011-0539-5