Iberian Lynx Lynx pardinus Temminck, 1827 (Mammalia: Carnivora: Felidae) in central Spain: trophic niche of an isolated population

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Pedro Alfaya
https://orcid.org/0000-0003-1405-0749
Ariadna Invernón
https://orcid.org/0000-0002-8503-2911
Germán Alonso
https://orcid.org/0000-0001-5933-2964

Abstract

Understanding predator-prey relationships is fundamental to develop effective conservation plans.  Between 2015 and 2018, we combed 21 transects, each 7km long, searching for Iberian Lynx Lynx pardinus scat within the province of Madrid in central Spain.  In order to minimise inherent subjectivity of visual identification as much as possible, we performed a double specific nested polymerase chain reaction (PCR) followed by a primer extension assay addressed to two Iberian Lynx diagnostic single nucleotide polymorphisms.  Forty-six scat samples were positively identified as belonging to Iberian Lynx through genetic analysis.  From these, we extracted remains of consumed prey, which we determined to the lowest possible taxonomic level, mainly through hair identification.  Identified prey was divided into four types: lagomorphs, small mammals, birds, and ungulates.  The species’ diet composition was described based on the frequency of occurrence (FO) of each prey and niche breadth, and also compared with prior knowledge of the species using four prior studies as a comparative reference through the calculation of the niche overlap value.  The FO of lagomorphs (39%) was the lowest, while the FO of small mammals (54%) was the highest recorded to date.  The niche breath (0.36) was higher than recorded in prior studies, but still showing the specialist character of the Iberian Lynx.  Niche overlap was low (C = 0.49), showing differences in trophic niche between the population in our study area and the one studied in southern Spain.  This indicates that the Iberian Lynx is adept at switching its main prey, an ability that has previously been firmly rejected.  It is, however, capable of adapting to alternative prey more often than recorded to date, which could be a behavioural response to the patchy distribution of European Rabbit Oryctolagus cuniculus in the study area.

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Communications

References

Alfaya, P., J.G. Casanovas, J. Lobón-Rovira, B. Matallanas, A. Cruz, P. Arana & G. Alonso (2019). Using MaxEnt algorithm to assess habitat suitability of a potential Iberian Lynx population in central Iberian Peninsula. Community Ecology 20(3): 266–267. https://doi.org/10.1556/168.2019.20.3.7 DOI: https://doi.org/10.1556/168.2019.20.3.7

Araujo, M.S., D.I. Bolnick & C.A. Layman (2011). The ecological causes of individual specialisation. Ecology Letters 14: 948–958. https://doi.org/10.1111/j.1461-0248.2011.01662.x DOI: https://doi.org/10.1111/j.1461-0248.2011.01662.x

Arnaiz-Schmitz, C., P. Díaz, D. Ruiz-Labourdette, C. Herrero-Jáuregui, M. Molina, C. Montes, F.D. Pineda & M.F. Schmitz (2018). Modelling of socio-ecological connectivity. The rural-urban network in the surroundings of Madrid (Central Spain). Urban Ecosystems 21: 1199–1212. https://doi.org/10.1007/s11252-018-0797-z DOI: https://doi.org/10.1007/s11252-018-0797-z

Aymerich, M. (1982). Étude comparative des régimes alimentaires du Lynx Pardelle (Lynx pardina) et du Chat Sauvage (Felis sylvestris). Mammalia 46(4): 515–521. https://doi.org/10.1515/mamm.1982.46.4.515 DOI: https://doi.org/10.1515/mamm.1982.46.4.515

Beltrán, J.F. & M. Delibes (1991). Ecología trófica del Lince Ibérico en Doñana durante un periodo seco. Doñana Acta Vertebrata 18(1): 113–122.

Beltrán, J.F. & M. Delibes (1994). Environmental determinants of circadian activity of free-ranging Iberian Lynxes. Journal of Mammalogy 75(2): 382–393.

Beltrán, J.F., C.S. José, M. Delibes & F. Braza (1985). An analysis of the Iberian Lynx predation upon Fallow Deer in the Coto Donana, SW Spain, pp. 961–967. In: Crombrugghe, S. (ed.). Transactions of XVIIth Congress of the International Union of Game Biologists. Ministry of Agriculture, Agricultural Research Administration Brussels, 1155pp.

Blanco, J.C. & R. Villafuerte (1993). Factores ecológicos que influyen sobre las poblaciones de Conejos. Incidencia de la enfermedad hemorrágica. Internal Technical Report Empresa de Transformación Agraria S.A.: 1–122.

Bolnick, D.I., R. Svanbäck, J.A. Fordyce, L.H. Yang, J.M. Davis, C.D. Hulsey & M.L. Forister (2003). The ecology of individuals: incidence and implications of individual specialisation. The American Naturalist 161(1): 1–28.

Boshoff, A.F. & G.I. Kerley (2010). Historical mammal distribution data: How reliable are written records? South African Journal of Science 106(1–2): 26–33. DOI: https://doi.org/10.4102/sajs.v106i1/2.116

Cabezas-Díaz, S., J. Lozano & E. Virgós (2009). The decline of the wild Rabbit (Oryctolagus cuniculus) and the Iberian Lynx (Lynx pardinus) in Spain: redirecting conservation efforts, pp. 283–310. In: Aranoff, J.B. (ed.). Handbook of Nature Conservation: Global, Environmental and Economic Issues. Nova Science Publishers, New York, 479pp.

Calvete, C., R. Estrada, E. Angulo & S. Cabezas-Ruiz (2004). Habitat factors related to wild Rabbit conservation in an agricultural landscape. Landscape Ecology 19: 531–542. https://doi.org/10.1023/B:LAND.0000036139.04466.06 DOI: https://doi.org/10.1023/B:LAND.0000036139.04466.06

Calzada, J. & F. Palomares (1996). Frecuencia de aparición de diferentes restos de conejo en excrementos de Lince y Zorro. Doñana Acta Vertebrata 23(2): 243–252.

Calzada, J., P. Muñoz, A. Sánchez, M.J. Palacios, C. Dávila, M.A. Simón, R. Cadenas, A. Leiva, S. Saldaña, F. Jiménez, R. Carbonell, J.I. Molina, A. Aranda, I. Mosqueda, L. Prada, L.M. González, B. Heredia, M. Aymerich, F.G. Domínguez, M. Delibes, F. Palomares, J.A. Godoy, A. Píriz, J. Calzada, A. Vargas, F. Martínez, J.N. Guzmán, S. Centenera, P. Garzón & J.L. González (2007). Estrategia para la Conservación del Lince Ibérico (Lynx pardinus). Comisión Nacional de Protección de la Naturaleza, Madrid, 44pp.

Carro, F., M. Ortega & C. Soriguer (2019). Is restocking a useful tool for increasing Rabbit densities? Global Ecology and Conservation 17: e00560. https://doi.org/10.1016/j.gecco.2019.e00560 DOI: https://doi.org/10.1016/j.gecco.2019.e00560

Colwell, R.K. & D.J. Futuyma (1971). On the measurement of niche breadth and overlap. Ecology 52(4): 567–576.

Costa, G.C., D.O. Mesquita, G.R. Colli & L.J. Vitt (2008). Niche expansion and niche variation hypothesis: does the degree of individual variation increase in depauperate assemblages? The American Naturalist 172(6): 868–877. DOI: https://doi.org/10.1086/592998

Cruz, A., B. Matallanas, J. Lobón-Rovira, J.G. Casanovas, G. Alonso & P. Arana (2019). Double specific nested PCR and diagnostic SNP assay for species identification in lynx fecal critical samples. Conservation Genetics Resources 11(2): 173–175. https://doi.org/10.1007/s12686-018-0993-4 DOI: https://doi.org/10.1007/s12686-018-0993-4

Delibes, M. (1977). Ecología y comportamiento alimenticio de Lynx pardina (Temminck 1824) en el coto de Doñana. PhD Thesis. Universidad Autónoma de Madrid, Madrid.

Delibes, M. (1980). Feeding Ecology of the Spanish Lynx in the Coto Doñana. Acta Theriologica 25(24): 309–324.

Delibes, M., F. Palacios, J. Garzónz & J. Castroviejo (1975). Notes sur l’alimentation et la biologie du Lynx Pardelle (Lynx pardina Temminck, 1824) en Espagne. Mammalia 39: 387–393.

Dove, C.J. & S.L. Koch (2011). Microscopy of feathers: a practical guide for forensic feather identification. The Microscope 59(2): 51–71.

Fedriani, J.M, F. Palomares & M. Delibes (1999). Niche relations among three sympatric Mediterranean carnivores. Oecologia 121(1): 138–148. https://doi.org/10.1007/s004420050915 DOI: https://doi.org/10.1007/s004420050915

Ferrer, M. & J.J. Negro (2004). The enar extinction of two large European predators: super specialists pay a price. Conservation Biology 18(2): 344–349. https://doi.org/10.1111/j.1523-1739.2004.00096.x DOI: https://doi.org/10.1111/j.1523-1739.2004.00096.x

Ferreras, P., A. Travaini, S.C. Zapata & M. Delibes (2011). Short-term responses of mammalian carnivores to a sudden collapse of Rabbits in Mediterranean Spain. Basic and Applied Ecology 12(2): 116–124. https://doi.org/10.1016/j.baae.2011.01.005 DOI: https://doi.org/10.1016/j.baae.2011.01.005

Garrote, G. & R.P. de Ayala (2015). Assessing unverified observation data used for estimating Iberian Lynx distribution. European Journal of Wildlife Research 61(5): 801–806. https://doi.org/10.1007/s10344-015-0941-5 DOI: https://doi.org/10.1007/s10344-015-0941-5

Garrote, G., R.P. de Ayala & J.L. Tellería (2014). A comparison of scat counts and camera-trapping as means of assessing Iberian Lynx abundance. European Journal of Wildlife Research 60(6): 885–889. https://doi.org/10.1007/s10344-014-0855-7 DOI: https://doi.org/10.1007/s10344-014-0855-7

Gastón, A., S. Blázque-Cabrera, G. Garrote, M.C. Mateo-Sánchez, P. Beier, M.A. Simón & S. Saura (2016). Response to agriculture by a woodland species depends on cover type and behavioural state: insights from resident and dispersal Iberian Lynx. Journal of Applied Ecology 53 (3): 814–824. https://doi.org/10.1111/1365-2664.12629 DOI: https://doi.org/10.1111/1365-2664.12629

Gil-Sánchez, J.M., E. Ballesteros-Duperón & J.F. Bueno-Segura (2006). Feeding ecology of the Iberian Lynx Lynx pardinus in eastern Sierra Morena (southern Spain). Acta Theriologica 51(1): 85–90. https://doi.org/10.1007/BF03192659 DOI: https://doi.org/10.1007/BF03192659

Guzmán, J.N., F.J. García, G. Garrote, R. Pérez & C. Iglesias (2004). Capítulo VI. Sínteis y Discusión, pp. 133–138. In: El Lince Ibérico (Lynx pardinus) en España y Portugal. Censo-diagnóstico de sus poblaciones. Dirección General para la Biodiversidad, Madrid, 174pp.

Hutchinson, G.E. (1957). Concluding remarks. Cold Spring Quantitative Biology 22: 415–427.

Iglesias, A. & A.J. España (eds.) (2010). Rastros y huellas de carnívoros ibéricos. Ediciones Jaguar, Spain, 350pp.

Klare, U., J.F. Kamler & D.W. Macdonald (2011). A comparison and critique of different scatâ€analysis methods for determining carnivore diet. Mammal Review 41(4): 294–312. https://doi.org/10.1111/j.1365-2907.2011.00183.x DOI: https://doi.org/10.1111/j.1365-2907.2011.00183.x

Krofel, M., D. Huber & M. Kos (2011). Diet of the Eurasian Lynx Lynx lynx in the northern Dinaric Mountains (Slovenia and Croatia). Acta Theriologica 56: 315–322. https://doi.org/10.1007/s13364-011-0032-2 DOI: https://doi.org/10.1007/s13364-011-0032-2

Levins, R. (1968). Evolution in Changing Environments. Princeton University Press, Princeton, 120pp.

Lozano, J., E. Virgós & S. Cabezas-Díaz (2013). Monitoring European Wildcat Felis silvestris populations using scat surveys in central Spain: are population trends related to wild Rabbit dynamics or to landscape features? Zoological Studies 52: 16. https://doi.org/10.1186/1810-522X-52-16 DOI: https://doi.org/10.1186/1810-522X-52-16

Martín, J., R. Grande, A. Hernando, J. Garzón, J. Eliseo, J. Echegaray, P. García-Buendía, J.G. González-Vázquez, A. Gutierrez, J.A. Manzanedo, F.M. de Lecea, J. Moro, J. Porras, J. Nicolás & J.C. Zamarreño (2007). Prospección del Lince Ibérico en los montes del centro de España. Fundación Abertis, Cantabria, 26pp.

Molinari-Jobin, A., M. Kéry, E. Marboutin, P. Molinari, I. Koren, C. Fuxjäger, C. Breitenmoserâ€Würsten, S. Wölfl, M. Fasel, I. Kos, M. Wölfl & U. Breitenmoser (2012). Monitoring in the presence of species misidentification: the case of the Eurasian Lynx in the Alps. Animal Conservation 15(3): 266–273. https://doi.org/10.1111/j.1469-1795.2011.00511.x DOI: https://doi.org/10.1111/j.1469-1795.2011.00511.x

Nájera, F., S. Sánchez-Cuerda, G. López, T. del Rey-Wamba, C. Rueda, N. Vallverdú-Coll, J. Panadero, M.J. Palacios, J.V. López-Vao & J. Jiménez (2019). Lynx eats cat: disease risk assessment during an Iberian Lynx intraguild predation. European Journal of Wildlife Research 64: 39. https://doi.org/10.1007/s10344-019-1275-5 DOI: https://doi.org/10.1007/s10344-019-1275-5

Palomares, F., M. Delibes, E. Revilla, J. Calzada & J.M. Fedriani (2001). Spatial ecology of Iberian Lynx and abundance of European Rabbits in southwestern Spain. Wildlife Monographs 148: 1–36.

Palomares, F., J.A. Godoy, A. Píriz & S.J. O’Brien (2002). Faecal genetic analysis to determine the presence and distribution of elusive carnivores: design and feasibility for the Iberian Lynx. Molecular Ecology 11(10): 2171–2182. https://doi.org/10.1046/j.1365-294X.2002.01608.x DOI: https://doi.org/10.1046/j.1365-294X.2002.01608.x

Popp, J.N., J. Hamr, J.L. Larkin & F.F. Mallory (2018). Black Bear (Ursus americanus) and Wolf (Canis spp.) summer diet composition and ungulate prey selectivity in Ontario, Canada. Mammal Research 63: 433–441. https://doi.org/10.1007/s13364-018-0368-y DOI: https://doi.org/10.1007/s13364-018-0368-y

Rivas, A., J. Boixader, A. Vargas, M.J. Pérez, R. Serra, V. Asensio, I., Sánchez, V. Lobato, A. Vázquez, A.J. Pardo, J.M. Chaparro, L. Penabad, J. Reeves, O.M. Jiménez, C. Ferreira, J. Yerga, N. Gonçalves, A. Azevedo, L. Ferreira, J.L. Mendoza, R. González, J. Martín, A. Mamán, E. Díaz. J. Gañán, R. Canales, C. Rojo, J.M. Aguilar, M.J. Coca, M. Cuadrado, L. Flores, M.A. Quevedo, J. Valkenburg, J. Pechém, M. Moreira, M. Fjaere, T. Costa, T. Lopes, N. Sánchez, V. Requeijão, V. Madeira, A. Grancho, S. Agudo, S. Casado, M.J. Fernández, F.J. Gil, L. González, M. González, J.M. Hebrero, A. López, J. Ramírez, L. Coloma, D. Martín, A.A. Esteban, A. Martínez-Cifuentes, A. Martínez-Martín, A. Flores, S. Ruiz, E. Parra, J. Sánchez, O. Muñoz, J. Bergara, F. Martínez & L. Klink. (2016). Manual de manejo del Lince Ibérico en cautividad. Grupo Asesor de Manejo en Cautividad del Comité de Cría del Lince Ibérico. Programa de Conservación Ex-situ del Lince Ibérico, Jeréz de la Frontera, 248pp.

Rivas-Martínez, S. (1982). Memoria del mapa de las series de vegetación de la provincia de Madrid. Escala 1:200,000. Servicio Forestal, del Medio Ambiente y Contra Incendios, Diputación de Madrid, 47pp.

Rodríguez, A. & J. Calzada (2015). Lynx pardinus. The IUCN Red List of Threatened Species 2015: e.T12520A50655794. Downloaded on 08 February 2020. https://doi.org/10.2305/IUCN.UK.2015-2.RLTS.T12520A50655794.en DOI: https://doi.org/10.2305/IUCN.UK.2015-2.RLTS.T12520A50655794.en

Rodríguez, A. & M. Delibes (1992). Current range and status of the Iberian Lynx Felis pardina Temminck, 1824 in Spain. Biological Conservation 61(3): 189–196.

Rodríguez, J.L. (1993). Guía de campo de los mamíferos terrestres de España. Ediciones Omega, Barcelona, 314pp.

Sáez-Gómez, P., S. Palacios & C. Camacho (2018). Landscape change promotes the emergence of a rare predator-prey interaction. Food Webs 15: e00078. https://doi.org/10.1016/j.fooweb.2018.e00078 DOI: https://doi.org/10.1016/j.fooweb.2018.e00078

San Miguel, A. (Coord.) (2006). Manual para la gestión del hábitat del Lince Ibérico (Lynx pardinus Temminck) y de su presa principal, el Conejo de Monte (Oryctolagus cuniculus L.). 1ª Reimpresión, Fundación CBD-Habitat, Madrid, 263pp.

Schmitz, M.F., I. de Aranzabal & F.D. Pineda (2007). Spatial analysis of visitor preferences in the outdoor recreational niche of Mediterranean cultural landscapes. Environmental Conservation 34(4): 300–312. https://doi.org/10.1017/S0376892907004249 DOI: https://doi.org/10.1017/S0376892907004249

Schoener, T.W. (1970). Nonsynchronous spatial overlap of lizards in patchy habitats. Ecology 51(3): 408–418.

Shipley, L.A., J.S. Forbey & B.D. Moore (2009). Revisiting the dietary niche: when is a mammal herbivore a specialist? Integrative and Comparative Biology 49(3): 274–290. https://doi.org/10.1093/icb/icp051 DOI: https://doi.org/10.1093/icb/icp051

Short, L.H. (1978). Analysis of cuticular scales on hairs using the scanning electron microscope. Journal of Mammalogy 59(2): 261–268.

Simón, M.A. (2018). Censo de las poblaciones Andaluzas de Lince Ibérico año 2017. Life+ Iberlince, Junta de Andalucía, Sevilla, 11pp.

Simón, M.A., J.M. Gil-Sánchez, G. Ruiz, G. Garrote, E.B. McCain, L. Fernández, M. López-Parra, E. Rojas, R. Arenas-Rojas, T. del Rey, M. García-Tardío & G. López. (2011). Reverse of the decline of the endangered Iberian Lynx. Conservation Biology 26(4): 731–736. https://doi.org/10.1111/j.1523-1739.2012.01871.x DOI: https://doi.org/10.1111/j.1523-1739.2012.01871.x

Smith, E.P. (1982). Niche breadth, resource availability and inference. Ecology 63(6): 1675–1681.

Soriguer, R.C. & F. Palacios (1994). Los lagomorfos ibéricos: liebres y conejos, pp. 63–82. In: García-Granados, A. & L. de Hierro (eds.). Curso de Gestión y Ordenación Cinegética. Colegio Oficial de Biólogos, Granada, 242pp.

Symondson, W.O.C., K.D. Sunderland & M.H. Greenstone (2002). Can generalist predators be effective biocontrol agents? Annual Review of Entomology 47(1): 561–594. https://doi.org/10.1146/annurev.ento.47.091201.145240 DOI: https://doi.org/10.1146/annurev.ento.47.091201.145240

Tapia, L., J. Domínguez, A. Regos & M. Vidal (2014). Using remote sensing data to model European wild Rabbit (Oryctolagus cuniculus) occurrence in a highly fragmented landscape in northwestern Spain. Acta Theriologica 59: 289–298. https://doi.org/10.1007/s13364-013-0169-2 DOI: https://doi.org/10.1007/s13364-013-0169-2

Teerink, B.J. (1991). Hair of west European mammals: Atlas and Identification Key. Cambridge University Press, Cambridge, 224pp.

Terraube, J. & B. Arroyo (2011). Factors influencing diet variation in generalist predator across its range distribution. Biodiversity and Conservation 20: 2111–2131. https://doi.org/10.1007/s10531-011-0077-1 DOI: https://doi.org/10.1007/s10531-011-0077-1

Torres, R.T., N. Silva, G. Brotas & C. Fonseca (2015). To eat or not to eat? The diet of endangered Iberian Wolf (Canis lupus signatus) in a human-dominated landscape in central Portugal. PLoS ONE 10 (6): e0129379. https://doi.org/10.1371/journal.pone.0129379 DOI: https://doi.org/10.1371/journal.pone.0129379

Valente, A.M., R.G. Rocha, E. Lozano, J.P. Ferreira & C. Fonseca (2015). Atlas dos Pelos dos Mamíferos Terrestres Ibéricos. Ediçoes Afrontamento, Porto, 188pp.

Valverde, J.A. (1963). Información sobre el Lince Ibérico en España. Boletín técnico, serie cinegética. Spanish Agricultural Ministry, Madrid, 37pp.

Villafuerte, R. (2007). Oryctolagus cuniculus (Linnaeus, 1758). Ficha Libro Rojo, pp. 487–491. In: Palomo, L.J., J. Gisbert & J.C. Blanco (eds). Atlas y Libro Rojo de los Mamíferos terrestres de España. Dirección General para la Biodiversidad SECEM-SECEMU, Madrid, 588pp.

Virgós, E., S. Cabezas-Díaz, A. Malo, J. Lozano & D. López-Huertas (2003). Factors shaping European Rabbit abundance in continuous and fragmented populations of central Spain. Acta Theriologica 48(1): 113–122. https://doi.org/10.1007/BF03194271 DOI: https://doi.org/10.1007/BF03194271

Wachter, B., A.S. Blanc, J. Melzheimer, O.P. Höner, M. Jago & H. Hofer (2012). An advanced method to assess the diet of free-ranging large carnivores based on scats. PLoS One 7: e38066. https://doi.org/10.1371%2Fjournal.pone.0038066 DOI: https://doi.org/10.1371/journal.pone.0038066

Zabía, M. & L. del Olmo (2007). Atlas Medio Ambiente de la Comunidad de Madrid. Consejería de Medio Ambiente y Ordenación del Territorio, Madrid, 83pp.