Abstract
The use of scats is a widespread non-invasive method in ecological studies of mammalian carnivores. However, their low detectability and the incorrect species assignment may be important sources of bias. We aimed to optimize the detection and identification of scats of Egyptian mongoose (Herpestes ichneumon), using the red fox (Vulpes vulpes) as a comparative model. Based on molecular identification of scats we assessed: (1) the accuracy of species morphological identification (Field-ID); (2) whether post-field laboratory analyses (FL-ID) improve Field-ID; (3) species-specific morphological differences of scats, and (4) whether specific field surveys increase the detectability of mongoose scats. Out of 175 collected scats, 81 were genetically identified. Field-ID accuracy was over 75.6% for the mongoose and over 45.0% for the red fox. Misidentified mongoose scats mainly belonged to stone marten (50.0%) while misidentified red fox scats mainly belonged to mongoose (63.6%). After applying FL-ID, accuracy increased to 93.1% for the Egyptian mongoose and 76.2% for the red fox. Morphological scat differences were only significant for the scat diameter, with red fox scats being significantly thicker than those of mongoose. More mongoose scats were found along ecotones (mean ± SE: 4.05 ± 1.45 scats/transect) than along trails and roads (0.05 ± 0.05 scats/transect), while red fox scats were found similarly in both transect types. The application of post-field analysis to scats and focusing the search along ecotones optimized both the identification accuracy and the detection probability of Egyptian mongoose scats, although searching for scats in other structures should not be discarded if the aim is the study of habitat use or selection by the species. Our results can be useful for scat identification in studies on this and other carnivore species.
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References
Alarcos G (2018) Nueva cita de meloncillo Herpestes ichneumon (Linnaeus, 1758) en el límite entre Salamanca y Zamora. Galemys 30:61–62
Alberts CC, Saranholi BH, Frei F, Galetti PM Jr (2017) Comparing hair-morphology and molecular methods to identify fecal samples from Neotropical felids. PLoS ONE 12:e0184073
Bandeira V, Virgós E, Carvalho J, Barros T, Cunha MV, Fonseca C (2018) Diet footprint of Egyptian mongoose along ecological gradients: effects of primary productivity and life history traits. Mamm Biol 88:16–25
Barea-Azcón JM, Virgós E, Ballesteros-Duperon E, Moleón M, Chirosa M (2007) Surveying carnivores at large spatial scales: a comparison of four broad-applied methods. Biodivers Conserv 16:1213–1230
Barja I, De Miguel FJ, Bárcena F (2001) Distribución espacial de los excrementos de zorro rojo (Vulpes vulpes, Linnaeus, 1758) en los Montes do Invernadeiro (Ourense). Galemys 13:171–178
Barros T, Fonseca C (2011) Expansão do sacarrabos Herpestes ichneumon (Linnaeus, 1758) em Portugal. Galemys 23:9–15
Barrull J, Mate I, Ruiz-Olmo J, Casanovas JG, Gosálbez J, Salicru M (2014) Factors and mechanisms that explain coexistence in a Mediterranean carnivore assemblage: an integrated study based on camera trapping and diet. Mamm Biol 79:123–131
Bates D, Mächler M, Bolker B, Walker S (2014) Fitting linear mixed-effects models using lme4. arXiv prepint arXiv: 1406.5823.
Beja-Pereira A, Oliveira R, Alves PC, Schwartz MK, Luikart G (2009) Advancing ecological understandings through technological transformations in noninvasive genetics. Mol Ecol Resour 9:1279–1301
Bencatel J, Álvares F, Moura AE, Barbosa AM (2017) Atlas de Mamíferos de Portugal. Universidade de Évora, Évora
Blanco JC (1998) Mamíferos de España. Ediciones Planeta, Barcelona
Broquet T, Ménard N, Petit E (2007) Noninvasive population genetics: a review of sample source, diet, fragment length and microsatellite motif effects on amplification success and genotyping error rates. Conserv Genet 8:249–260
Cecere JG, Benedetti MC, Guj I, Imperio S (2014) The role of the red fox as a predator of species of human concern in a Mediterranean rural habitat: a case study. Russ J Ecol 45:555–558
Chame M (2003) Terrestrial mammal feces: a morphometric summary and description. Memórias do Instituto Oswaldo Cruz 98:71–94
Davison A, Birks JDS, Brookes RC, Braithwaite TC, Messenger JE (2002) On the origin of faeces: morphological versus molecular methods for surveying rare carnivores from their scats. J Zool 257:141–143
Delibes-Mateos M, Fernandez de Simon J, Villafuerte R, Ferreras P (2008) Feeding responses of the red fox (Vulpes vulpes) to different wild rabbit (Oryctolagus cuniculus) densities: a regional approach. Eur J Wildl Res 54:71–78
Díaz-Ruiz F, Delibes-Mateos M, García-Moreno JL, María López-Martín J, Ferreira C, Ferreras P (2013) Biogeographical patterns in the diet of an opportunistic predator: the red fox Vulpes vulpes in the Iberian Peninsula. Mamm Rev 43:59–70
Espírito-Santo C, Rosalino LM, Santos-Reis M (2007) Factors affecting the placement of common genet latrine sites in a Mediterranean landscape in Portugal. J Mammal 88:201–207
Fernandes CA, Ginja C, Pereira I, Tenreiro R, Bruford MW, Santos-Reis M (2008) Species-specific mitochondrial DNA markers for identification of non-invasive samples from sympatric carnivores in the Iberian Peninsula. Conserv Genet 9:681–690
Fernandez de Simon J, Díaz-Ruiz F, Rodríguez-de la Cruz M, Delibes-Mateos M, Villafuerte R, Ferreras P (2015) Can widespread generalist predators affect keystone prey? A case study with red foxes and European rabbits in their native range. Popul Ecol 57:591–599
Ferreras P, Travaini A, Zapata SC, Delibes M (2011) Short-term responses of mammalian carnivores to a sudden collapse of rabbits in Mediterranean Spain. Basic Appl Ecol 12:116–124
Gaubert P, Machordom A, Morales A, López-Bao JV, Veron G, Amin M, Barros T, Basuony M, Djagoun CAMS, San EDL, Fonseca C, Geffen E, Ozkurt SO, Cruaud C, Couloux A, Palomares F (2011) Comparative phylogeography of two African carnivorans presumably introduced into Europe: disentangling natural versus human-mediated dispersal across the Strait of Gibraltar. J Biogeogr 38:341–358
Gittleman JL, Funk SM, MacDonald DW, Wayne RK (2001) Carnivore conservation. Cambridge University Press, Cambridge
González-Broco C, Vázquez J, Larios-López JE, Fernández A, Cortés S, Blanca I, Santiago JS, Sacramento J, Castillo S, Fernández-Cardenete JR, Vadillo A, Bautista J, Jaramillo J, Barea-Azcón JM, Virgós E (2016) Distribución del meloncillo (Herpestes ichneumon) en la provincia de Granada. Galemys 28:41–51
Gross J, Ligges U (2015) nortest: tests for normality. R package version 1.0-4. https://CRAN.R-project.org/package=nortest.
Güthlin D, Kröschel M, Küchenhoff H, Storch I (2012) Faecal sampling along trails: a questionable standard for estimating red fox Vulpes vulpes abundance. Wildl Biol 18:374–383
Hämäläinen A, Broadley K, Droghini A, Haines JA, Lamb CT, Boutin S, Gilbert S (2017) The ecological significance of secondary seed dispersal by carnivores. Ecosphere 8:e01685
Harrington LA, Harrington AL, Hughes J, Stirling D, Macdonald DW (2010) The accuracy of scat identification in distribution surveys: American mink, Neovison vison, in the northern highlands of Scotland. Eur J Wildl Res 56:377–384
Heinemeyer KS, Ulizio TJ, Harrison RL (2008) Natural sign: tracks and scats. In: Long RA, MacKay P, Zielinski WJ, Ray JC (eds) Noninvasive survey methods for carnivores. Island Press, Washington D.C., pp 45–74
Iglesias A, España AJ (2010) Rastros y huellas de los carnívoros ibéricos. Ediciones Jaguar, Madrid
Jiménez J, Nuñez-Arjona JC, Mougeot F, Ferreras P, González LM, García-Domínguez F, Muñoz-Igualada J, Palacios MJ, Pla S, Rueda C, Villaespesa F, Nájera F, Palomares F, López-Bao JV (2019) Restoring apex predators can reduce mesopredator abundances. Biol Conserv 238:108234
Kamler JF, Stenkewitz U, Klare U, Jacobsen NF, Macdonald DW (2012) Resource partitioning among cape foxes, bat-eared foxes, and black-backed jackals in South Africa. J Wildl Manag 76:1241–1253
Kluever BM, Gese EM, Dempsey SJ (2015) The influence of road characteristics and species on detection probabilities of carnivore faeces. Wildl Res 42:75–82
Linares O, Carranza J, Soliño M, Delibes-Mateos M, Ferreras P, Descalzo E, Martínez-Jauregui M (2020) Citizen science to monitor the distribution of the Egyptian mongoose in southern Spain: who provide the most reliable information? Eur J Wild Res 66(4):1–5
Lonsinger RC, Gese EM, Waits LP (2015) Evaluating the reliability of field identification and morphometric classifications for carnivore scats confirmed with genetic analysis. Wildl Soc Bull 39:593–602
Macdonald DW (1980) Patterns of scent marking with urine and faeces amongst carnivore communities. Symp Zool Soc Lond 45:107–139
Martínez-Jauregui M, Linares O, Carranza J, Soliño M (2017) Dealing with conflicts between people and colonizing native predator species. Biol Conserv 209:239–244
Miotto RA, Ciocheti G, Rodrigues FP, Galetti PM Jr (2007) Identification of pumas (Puma concolor (Linnaeus, 1771)) through faeces: a comparison between morphological and molecular methods. Braz J Biol 67:963–965
Monterroso P (2006) Distribuição, selecção de habitat e actividade do gato-bravo (Felis silvestris) no Parque Natural do Vale Do Guadiana. MSc thesis, University of Oporto, Oporto
Monterroso P, Castro D, Silva TL, Ferreras P, Godinho R, Alves PC (2013) Factors affecting the (in) accuracy of mammalian mesocarnivore scat identification in South-western Europe. J Zool 289:243–250
Moral M, Prunier F, Saldaña S (2014) Meloncillo Herpestes icheneumon (Linnaeus, 1758). In: Calzada J., Clavero, M., Fernández, A. (Eds) Guía virtual de los indicios de los mamíferos de la Península Ibérica, Islas Baleares y Canarias. Sociedad Española para la Conservación y Estudio de los Mamíferos (SECEM). https://www.secem.es/guiadeindiciosmamiferos/. Accessed 28 Mar 2020.
Oliveira R, Castro D, Godinho R, Luikart G, Alves PC (2010) Species identification using a small nuclear gene fragment: application to sympatric wild carnivores from South-western Europe. Conserv Genet 11:1023–1032
Palomares F (1993) Faecal marking behaviour by free-ranging common genets Genetta genetta and Egyptian mongooses Herpestes ichneumon in southwestern Spain. Z Säugetierkd 58:225–231
Palomares F (2007) Herpestes ichneumon (Linnaeus, 1758). In: Palomo LJ, Gisbert J, Blanco JC (eds) Atlas y Libro Rojo de los Mamíferos terrestres de España. Dirección General para la Biodiversidad-SECEM-SECEMU, Madrid, pp 327–329
Palomares F (2017) Meloncillo–Herpestes ichneumon. In: Salvador, A., Barja, I. (Eds) Enciclopedia Virtual de los Vertebrados Españoles. Museo Nacional de Ciencias Naturales, Madrid. https://www.vertebradosibericos.org/. Accessed 28 Mar 2020.
Palomares F, Caro TM (1999) Interspecific killing among mammalian carnivores. Am Nat 153:492–508
Palomares F, Gaona P, Ferreras P, Delibes M (1995) Positive effects on game species of top predators by controlling smaller predator populations: an example with lynx, mongoose and rabbits. Conserv Biol 9:295–305
Palomares F, Godoy JA, 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
Palomo LJ, Gisbert J, Blanco JC (2007) Atlas y Libro Rojo de los Mamíferos terrestres de España. Dirección General para la Biodiversidad-SECEM-SECEMU, Madrid
Panasci M, Ballard WB, Breck S, Rodriguez D, Densmore LD III, Wester DB, Baker RJ (2011) Evaluation of fecal DNA preservation techniques and effects of sample age and diet on genotyping success. J Wildl Manag 75:1616–1624
Pereira M, Rodríguez A (2010) Conservation value of linear woody remnants for two forest carnivores in a Mediterranean agricultural landscape. J Appl Ecol 47:611–620
Power ME (1992) Top-down and bottom-up forces in food webs: do plants have primacy. Ecology 73:733–746
Prugh LR, Stoner CJ, Epps CW, Bean WT, Ripple WJ, Laliberte AS, Brashares JS (2009) The rise of the mesopredator. Bioscience 59:779–791
Recio MR, Virgós E (2010) Predictive niche modelling to identify potential areas of conflicts between human activities and expanding predator populations: a case study of game management and the grey mongoose, Herpestes ichneumon, in Spain. Wildl Res 37:343–354
R Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/.
Redpath SM, Young J, Evely A, Adams WM, Sutherland WJ, Whitehouse A, Amar A, Lambert RA, Linnell JDC, Watt A, Gutiérrez RJ (2013) Understanding and managing conservation conflicts. Trends Ecol Evol 28:100–109
Reid RE (2015) A morphometric modeling approach to distinguishing among bobcat, coyote and gray fox scats. Wildl Biol 21:254–263
Reynolds J, Aebischer N (1991) Comparison and quantification of carnivore diet by faecal analysis: a critique with recommendations based on study of the Fox Vulpes vulpes. Mamm Rev 21:97–122
Ritchie EG, Johnson CN (2009) Predator interactions, mesopredator release and biodiversity conservation. Ecol Lett 12:982–998
Ritchie EG, Elmhagen B, Glen AS, Letnic M, Ludwig G, McDonald RA (2012) Ecosystem restoration with teeth: what role for predators? Trends Ecol Evol 27:265–271
Rosalino L, Santos M, Pereira I, Santos-Reis M (2009) Sex-driven differences in Egyptian mongoose’s (Herpestes ichneumon) diet in its northwestern European range. Eur J Wildl Res 55:293–299
Rosalino L, Santos-Reis M, Rosa S (2010) The role of carnivores as Mediterranean seed dispersers. Ann Zool Fenn 47:195–205
Rosellini S, Osorio E, Ruiz-González 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
Sadlier LM, Webbon CC, Baker PJ, Harris S (2004) Methods of monitoring red foxes Vulpes vulpes and badgers Meles meles: are field signs the answer? Mamm Rev 34:75–98
Santos T, Fonseca C, Barros T, Godinho R, Bastos-Silveira C, Bandeira V, Rocha RG (2015) Using stomach contents for diet analysis of carnivores through DNA barcoding. Wildl Biol Pract 11:31–39
Teerink BJ (1991) Hair of West-European mammals. Cambridge University Press, Cambridge
Terborgh J, Estes JA, Paquet P, Ralls K, Boyd-Herger D, Miller BJ, Noss RF (1999) The role of top carnivores in regulating terrestrial ecosystems. In: Soulé ME, Terborgh J (eds) Continental conservation: scientific foundations of regional reserve networks. Island Press, Washington, pp 39–64
Valente AM, Rocha RG, Lozano E, Ferreira JP, Fonseca C (2015) Atlas dos Pelos dos mamíferos terrestres ibéricos. Edições Afrontamento, Universidade do Aveiro, Aveiro
Vynne C, Baker MR, Breuer ZK, Wasser SK (2012) Factors influencing degradation of DNA and hormones in maned wolf scat. Anim Conserv 15:184–194
Webbon CC, Baker PJ, Harris S (2004) Faecal density counts for monitoring changes in red fox numbers in rural Britain. J Appl Ecol 41:768–779
Wilson GJ, Delahay RJ (2001) A review of methods to estimate the abundance of terrestrial carnivores using field signs and observation. Wildl Res 28:151–164
Woodroffe R, Thirgood S, Rabinowitz A (2005) People and wildlife, conflict or co-existence?. Cambridge University Press, Cambridge
Wysong ML, Tulloch AI, Valentine LE, Hobbs RJ, Morris K, Ritchie EG (2019) The truth about cats and dogs: assessment of apex-and mesopredator diets improves with reduced observer uncertainty. J Mammal 100:410–422
Zar JH (1999) Biostatistical analysis. The University of Chicago Press Upper Saddle River, New Jersey
Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. Springer, New York
Acknowledgements
This study is part of the project SBPLY/17/180501/000184, funded by the regional Government of Castilla-La Mancha and the European Regional Development Fund (ERDF). We are grateful for the support received by Ana Serronha and Elisa Maio during the fieldwork developed in Guadiana Valley Natural Park in Portugal. We especially thank P.C. Alves for the genetic analyses of scats performed at the CIBIO/InBIO laboratory of Porto University, as well as for the logistic support during the fieldwork at Guadiana Valley Natural Park. F. Díaz-Ruiz was supported by a postdoctoral contract financed by the European Social Fund (ESF) and Junta de Comunidades de Castilla-La Mancha (Operational Programme FSE 2007/2013) and by a “Juan de la Cierva” research contract (Ministerio de Ciencia e Innovación, Funder Id: 10.13039/501100004837, FJCI-2015-24949) from the Spanish Ministry of Economy, Industry and Competitiveness.
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This study is part of the project SBPLY/17/180501/000184, funded by the regional Government of Castilla-La Mancha and the European Regional Development Fund (ERDF).
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PF and FD-R conceived the ideas and designed methodology; JAT and FD-R collected the data; FD-R and JAT analysed the data; ED and FD-R led the writing of the manuscript. All authors contributed critically to the drafts and gave final approval for publication.
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Descalzo, E., Torres, J.A., Ferreras, P. et al. Methodological improvements for detecting and identifying scats of an expanding mesocarnivore in south-western Europe. Mamm Biol 101, 71–81 (2021). https://doi.org/10.1007/s42991-020-00062-6
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DOI: https://doi.org/10.1007/s42991-020-00062-6