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Ecología y gestión de depredadores generalistas: el caso del zorro (Vulpes
vulpes) y la urraca (Pica pica)
Memoria presentada por
Francisco Díaz Ruiz
para optar al grado de Doctor
VºBº Directores
Dr. Pablo Ferreras de Andrés Dr. Miguel Delibes Mateos
Instituto de Investigación en Recursos Cinegéticos (IREC-CSIC-UCLM-JCCM)
Departamento de Ciencia y Tecnología Agroforestal
Universidad de Castilla-La Mancha
1
Índice INTRODUCCIÓN GENERAL ................................................................................................. 4
Relación histórica entre hombres y depredadores ................................................................... 4
Impacto de la depredación en las presas: depredadores especialistas y generalistas ................ 6
Factores que favorecen a los depredadores generalistas ......................................................... 8
Ecología del zorro y la urraca: paradigma de especies generalistas ....................................... 11
El control de depredadores como herramienta de gestión y conservación ............................. 12
Efectos derivados del control de depredadores ..................................................................... 14
Efecto sobre las presas .................................................................................................... 14
Efecto sobre los depredadores generalistas objeto de control ............................................ 15
Efecto sobre especies que no son objeto de control .......................................................... 16
El control de depredadores en España .................................................................................. 18
Regulación legal del control de depredadores .................................................................. 20
Métodos de control de depredadores generalistas ............................................................. 21
Efectos del control de depredadores en España ................................................................ 23
OBJETIVOS Y ESTRUCTURA DE LA TESIS ...................................................................... 25
CAPÍTULO 1: Biogeographical patterns in the diet of an opportunistic predator: the red fox Vulpes vulpes in the Iberian Peninsula ..................................................................................... 27
Abstract .............................................................................................................................. 28
Introduction ........................................................................................................................ 29
Material and Methods ......................................................................................................... 32
Results ................................................................................................................................ 35
Discussion .......................................................................................................................... 40
Acknowledgements ............................................................................................................. 45
CAPÍTULO 2: Factors affecting the feeding habits of black-billed magpies Pica pica during the breeding season in Mediterranean Iberia.................................................................................. 46
Abstract .............................................................................................................................. 47
Introduction ........................................................................................................................ 48
Material and Methods ......................................................................................................... 49
Results ................................................................................................................................ 52
Discussion .......................................................................................................................... 58
Acknowledgements ............................................................................................................. 60
Ethical standards ................................................................................................................. 61
2
CAPÍTULO 3: An evaluation of cage-traps and the Collarum device to capture red foxes (Vulpes vulpes). Can the performance of cage-traps be improved by baits and scent attractants? ............................................................................................................................................... 62
Abstract .............................................................................................................................. 63
Introduction ........................................................................................................................ 65
Material and Methods ......................................................................................................... 67
Results ................................................................................................................................ 73
Discussion .......................................................................................................................... 81
Acknowledgements ............................................................................................................. 84
Ethical standards ................................................................................................................. 84
CAPÍTULO 4: Experimental evaluation of live cage-traps for Black-billed magpies Pica pica management in Spain .............................................................................................................. 85
Abstract .............................................................................................................................. 86
Introduction ........................................................................................................................ 87
Materials and Methods ........................................................................................................ 89
Results ................................................................................................................................ 94
Discussion ........................................................................................................................ 101
Acknowledgements ........................................................................................................... 103
Ethical standards ............................................................................................................... 104
CAPÍTULO 5: Assessing the influence of predator control on target and non-target predator populations using occupancy models ..................................................................................... 105
Abstract ............................................................................................................................ 106
Introduction ...................................................................................................................... 107
Material and Methods ....................................................................................................... 109
Results .............................................................................................................................. 114
Discussion ........................................................................................................................ 120
Acknowledgements ........................................................................................................... 123
Ethical standards ............................................................................................................... 123
CAPÍTULO 6: Drivers of red fox (Vulpes vulpes) daily activity: prey availability, human disturbance or habitat structure? ............................................................................................ 124
Abstract ............................................................................................................................ 125
Introduction ...................................................................................................................... 126
Material and Methods ....................................................................................................... 128
Results .............................................................................................................................. 133
Discussion ........................................................................................................................ 138
Acknowledgements ........................................................................................................... 140
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Ethical standards ............................................................................................................... 140
DISCUSIÓN GENERAL ...................................................................................................... 141
Ecología trófica del zorro y la urraca ................................................................................. 141
Evaluación y mejora de los métodos de captura para el control de zorros y urracas ............ 145
Efectos del control de depredadores sobre las poblaciones de zorros y urracas ................... 151
Efectos sobre otras especies no objeto de control ............................................................... 153
Efectos sobre el comportamiento de los depredadores objeto de control ............................. 155
Futuras líneas de investigación .......................................................................................... 156
CONCLUSIONES ................................................................................................................ 159
REFERENCIAS ................................................................................................................... 163
APÉNDICES ........................................................................................................................ 197
Appendix 1.1. ................................................................................................................... 198
Appendix 1.2 .................................................................................................................... 203
Appendix 2.1. ................................................................................................................... 208
Appendix 2.2. ................................................................................................................... 209
Appendix 2.3. ................................................................................................................... 210
Appendix 3.1. ................................................................................................................... 211
Appendix 3.2. ................................................................................................................... 214
Appendix 4.1. ................................................................................................................... 215
Appendix 5.1. ................................................................................................................... 216
Appendix 5.2. ................................................................................................................... 217
4
INTRODUCCIÓN GENERAL
Relación histórica entre hombres y depredadores El hombre tiene una larga historia de coexistencia con los depredadores que
probablemente comenzó como una relación depredador-presa, en la que los primeros
homínidos habrían sido presas de los grandes depredadores (Headland y Greene 2011;
Njau y Blumenschine 2012). El hombre, como presa, desarrolló en primer lugar un
sentimiento de temor ante los depredadores por riesgo a ser depredado. Con el paso del
tiempo, el hombre se convirtió en un eficiente depredador al aprender a utilizar diversas
herramientas que le confirieron la capacidad de defenderse de los depredadores y la
posibilidad de cazar grandes presas. (McCade y McCade 1984; Vargas 2002). Desde ese
momento, el hombre percibe a otros depredadores como competidores por alimentarse
de presas de interés humano (Conover 2002; Vargas 2002).
La persecución de los depredadores por parte del hombre pudo comenzar, por lo tanto,
hace muchísimos años por lo que se trataría de una actividad muy antigua, y extendida
por todo el mundo. Quizás los casos más conocidos sean los de los grandes carnívoros
como el lobo (Canis lupus) en Europa, Asia y América (Musiani y Paquet 2004; Sillero-
Zubiri y Schwitzer 2004) o los grandes felinos en África, Asia y América (Woodroffe y
Frank 2005; Balme et al. 2009; Inskip y Zimmerman 2009), los cuales consumen
diferentes especies de ganado o incluso atacan a los propios humanos (Treves y Karanth
2003). No obstante, existen también numerosos ejemplos de otros depredadores de
menor tamaño que han sido perseguidos por ser potenciales depredadores de especies de
caza menor, piscícolas, ganado e incluso por ser considerados como perjudiciales para
la agricultura. Entre estos destacan carnívoros de pequeña y mediana talla (Reynolds y
Tapper 1996; Virgós y Travaini 2005), rapaces en general (Villafuerte et al.1998;
Thirgood et al. 2000a; Whitfield et al. 2003, Whitfield et al. 2007) e incluso algunos
córvidos (Hadjisterkotis 2003; Madden et al. en prensa).
En este sentido España no ha sido una excepción, y la persecución de depredadores ha
sido una actividad muy extendida y arraigada desde hace mucho tiempo como así
acreditan diferentes documentos históricos. Archivos históricos constatan una
persecución organizada e impuesta de osos (Ursus arctos), lobos y zorros comunes
(Vulpes vulpes, zorro en adelante) ya desde la Edad Media (Vargas 2002). Pero quizás
5
el mejor ejemplo de la sistematización de esta persecución sea la creación a mediados
del siglo XX de las conocidas “Juntas provinciales de extinción de animales dañinos y
protección a la caza” promovidas y financiadas por la administración pública. La
finalidad de estas Juntas fue la erradicación de aquellas especies consideradas entonces
como dañinas, entre las que se incluían carnívoros, rapaces y córvidos, para la que no
existía ningún tipo de restricción en cuanto a los métodos utilizados (Vargas 2002;
Corbelle-Rico y Rico-Boquete 2008).
Esta persecución ejercida por el hombre ha contribuido al declive de algunas especies a
lo largo del tiempo (Langley y Yalden 1977; Villafuerte et al. 1998; Ripple et al. 2014).
En España la larga historia de persecución de depredadores contribuyó probablemente a
la regresión y rarefacción de las poblaciones de muchas especies de depredadores, como
el lobo (Valverde 1971; Blanco et al. 1992) o el lince ibérico (Lynx pardinus)
(Rodríguez y Delibes 2002; 2004) e incluso de grandes rapaces necrófagas como el
quebrantahuesos (Gypaetus barbatus), que desapareció por completo del sur de la
Península Ibérica (Hiraldo et al. 1979).
La percepción sobre parte de los depredadores comienza a cambiar entre mediados y
finales del siglo XX, al menos en aquellas regiones del planeta más desarrolladas. Esto
se debe en gran parte a al éxodo de personas del medio rural a las grandes urbes
industrializadas y a el inicio de una conciencia social sobre la conservación de la
biodiversidad (Conover et al. 2002), concepto que no será definido como tal hasta los
años 80 (Kareiva y Marvier 2012). En relación a esta nueva conciencia social de
conservación se crean nuevas medidas de protección para la fauna silvestre mediante
diferentes leyes y normativas que incluyen la protección de un número importante de
depredadores. Por ejemplo, en 1954 se promulgó en Reino Unido la Ley de Protección
de las Aves, según la cual un gran número de rapaces pasaron a ser especies protegidas
(Whitfield et al. 2003). Igualmente, en España este cambio de tendencia se ve reflejado
a finales de los años 60 con la aprobación de la Orden General de Vedas de 1966, que
prohíbe la caza de algunas especies consideradas nocivas hasta entonces como por
ejemplo el lince ibérico. Pocos años después, la de la Ley de caza de 1970 regula y
limita las especies que se pueden cazar así como las épocas y zonas para hacerlo
(Vargas 2002).
6
Posteriormente, en la Convención de Washington de 1973 sobre Comercio Internacional
de Especies Amenazadas de Flora y Fauna Silvestres (CITES) se redacta el primer
catálogo internacional de especies protegidas frente a la explotación comercial, en el
que se recogen un gran número de especies de depredadores. A pesar de la protección
legal de muchos de estos depredadores, la persecución ilegal de gran parte de ellos ha
continuado hasta nuestros días, como atestigua el reciente repunte del uso de cebos
envenenados para controlar estas especies (Márquez et al. 2013; Martínez-Abraín et al.
2013).
Aunque la percepción de los depredadores por la sociedad actual ha variado
considerablemente en el último siglo (Martínez-Abraín et al. 2008), ésta sigue
dependiendo de los intereses de diferentes grupos sociales o sectores. Así, la percepción
y actitudes hacia los depredadores es diferente entre los grupos interesados en la
conservación (p. ej. conservacionistas) y otros sectores con intereses productivos y de
explotación de especies que son potenciales presas para los depredadores, como los
ganaderos o cazadores (Treves y Bruskotter 2014). Algunos miembros de estos sectores
siguen considerando hoy en día que los depredadores son perjudiciales porque
consumen especies de cierto valor económico (Reynolds y Tapper, 1996; Graham et al.
2005). En ocasiones esto también ocurre porque se considera que los depredadores
pueden ser peligrosos para el propio hombre (Packer et al. 2005; Goodrich et al. 2011).
Hoy en día la problemática derivada de la actividad de los depredadores (es decir, los
daños ocasionados por la depredación) es a menudo gestionada mediante el control letal
de estos depredadores (en adelante, control de depredadores). Este se basa en la
eliminación de individuos de la especie “problemática” con la intención de reducir la
abundancia de sus poblaciones y disminuir de esta forma la presión de depredación
sobre las presas. Esta medida de gestión es fuente de conflicto entre los diferentes
sectores citados anteriormente, ya que su aplicación solo beneficia o satisface las
pretensiones de una de las partes implicadas en el conflicto, lo cual dificulta la
resolución de los mismos (Redpath et al. 2013).
Impacto de la depredación en las presas: depredadores especialistas y
generalistas Como se ha mencionado en la sección anterior, existe la creencia relativamente
extendida entre diferentes sectores de que los depredadores impactan negativamente
7
sobre las poblaciones de sus presas. Desde este punto de vista es importante conocer el
impacto real de la depredación sobre las presas. Para ello, en primer lugar se deben de
diferenciar los efectos de la depredación sobre el ganado, cuyas poblaciones están
controladas por el hombre, de los efectos sobre las poblaciones de presas silvestres. En
estas últimas, la dinámica poblacional está modulada por diferentes factores, tanto
intrínsecos (p. ej. estado fisiológico, genética, comportamiento social, competencia
intraespecífica) como extrínsecos (p. ej. hábitat, disponibilidad de alimento,
climatología, parásitos, enfermedades y depredación), que a menudo interactúan entre sí
(Sinclair y Pech 1996; Krebs 2002).
Los depredadores son, por lo tanto, un factor más en la dinámica de las poblaciones de
presas silvestres y sus efectos pueden ir desde la regulación (proceso por el que el
depredador devuelve a la población de la presa a su densidad de equilibrio) hasta la
limitación (proceso por el que el depredador establece la densidad de equilibrio de la
presa) de las poblaciones de presas (Krebs 2002). El balance positivo o negativo de
estos efectos sobre las presas depende en gran medida de la biología y abundancia de las
presas, la abundancia del propio depredador/es, así como de la biología y la ecológica
trófica de éste (Sinclair y Pech 1996; Sinclair et al. 2003). La teoría ecológica clasifica a
las especies en dos grandes grupos, especialistas y generalistas, en función de la
amplitud de nicho ecológico que presentan, definido este según varios ejes tanto
bióticos como abióticos (p. ej. alimentación, hábitat, climatología, altitud, etc.)
(Futuyma y Moreno 1988). Según esta teoría las especies especialistas presentarían una
reducida amplitud de nicho ecológico en la cual sus poblaciones pueden conseguir un
rendimiento ecológico óptimo, mientras que el nicho ecológico de las especies
generalistas presenta una mayor amplitud. En el caso concreto de los depredadores, se
distinguen depredadores generalistas, que tienen un amplio nicho trófico (alimentación
variada), y depredadores especialistas, con un nicho trófico reducido (poca variedad de
presas). No obstante, existen grupos ecológicos intermedios, como los denominados
depredadores especialistas facultativos, que pueden adaptar su estrategia a las
condiciones dominantes, cambiando su presa principal cuando otras presas más
rentables están disponibles (Glasser 1982).
Debido a su reducida amplitud trófica, los depredadores especialistas presentan cambios
en el tamaño poblacional asociados a la densidad de su principal presa (i.e. respuesta
numérica). Por ello no suelen representar un riesgo para las poblaciones de sus presas
8
(Begon et al. 1996), aunque existen algunas excepciones (ver p. ej. Hanski et al 1991).
Estas características les permiten un desarrollo óptimo en condiciones ambientales
estables y homogéneas, pero sin embargo, les limita considerablemente su capacidad de
respuesta ante cambios ambientales.
Por el contrario los depredadores generalistas presentan una serie de características
biológicas que les confieren una gran flexibilidad ecológica (Begon et al. 1996). Se
alimentan de varios tipos de presas en función de su abundancia, cambiando la tasa de
depredación sobre su presa principal ante la variación de la densidad de la misma (i.e.
respuesta funcional). Dicho de otro modo, pueden adaptarse a alimentarse de presas
secundarias cuando su principal presa disminuye de abundancia. Los depredadores
generalistas suelen presentar altas tasas de reproducción por lo que sus poblaciones
pueden llegar a ser abundantes.
El incremento en la abundancia de los depredadores generalistas puede provocar un
notable impacto negativo para algunas poblaciones de presas simplemente por el
aumento en el riesgo de depredación, es decir aumento de la depredación incidental
(Thirgood et al. 2000b; Valkama et al. 2005; Prugh et al. 2009; Eagan et al. 2011;
Ripple et al. 2013). Altas densidades de este tipo de depredadores pueden reducir e
incluso extinguir las poblaciones de ciertas presas, provocando importantes desajustes
en la estructura y estabilidad de las comunidades en las que se encuentran (Prugh et al.
2009).
Factores que favorecen a los depredadores generalistas
Actualmente gran parte de los sistemas naturales han sido fuertemente modificados por
la mano del hombre (Sanderson et al. 2002), lo que parece haber beneficiado a muchos
depredadores generalistas. Esto se debe principalmente al efecto combinado de la
rarefacción de depredadores apicales (del inglés top predators, depredadores claves en
la regulación de los procesos ecológicos de las comunidades de los que forman parte;
Sergio et al. 2008), a la modificación y fragmentación de hábitats y al incremento de
recursos alimentarios derivados de la actividad humana (Prugh et al. 2009).
Durante el pasado siglo las poblaciones de muchas especies de depredadores apicales se
han visto reducidas a escala mundial, debido principalmente a la persecución humana y
a la modificación y pérdida de sus hábitats o el de sus principales presas. Tal ha sido el
9
caso de grandes carnívoros como osos, lobos y grandes felinos en todo el mundo
(Ripple et al. 2014) y grandes rapaces como el águila real (Aquila chrysaetos)
(Whitfield et al. 2007) o el búho real (Bubo bubo) en algunas zonas de Europa
(Penteriani y Delgado 2010). En la Península Ibérica también existen dos casos muy
reconocidos, el lince ibérico y el águila imperial ibérica (Aquila adalberti) (Rodríguez y
Delibes 2002; 2004; González et al. 2008). Los depredadores apicales, muchos de ellos
considerados como especialistas, actúan como especies clave en los ecosistemas
limitando las poblaciones de otros depredadores menores, ya sea por depredación
directa o por exclusión competitiva (Palomares y Caro 1999; Sergio e Hiraldo 2008).
De esta manera, la presencia de depredadores apicales puede resultar beneficiosa para
sus presas al disminuir la tasa de depredación por depredadores de tamaño medio (los
llamados “mesodepredadores”) (Palomares et al. 1995; Sergio e Hiraldo 2008).
Ante este escenario de ausencia de depredadores apicales, los mesodepredadores a
menudo generalistas, pueden beneficiarse aumentando su abundancia y rango de
distribución según la denominada Hipótesis de “liberación de mesodepredadores” (del
inglés Mesopredator Release Hypothesis; Crooks y Soulé 1999). Numerosos estudios
han encontrado evidencias por todo el mundo que confirman esta hipótesis (Prugh et al.
2009; Ritchie y Johnson 2009). Algunos ejemplos son el aumento de coyotes en
Norteamérica tras la regresión de la poblaciones de lobos (Ripple et al. 2013), la
limitación de las poblaciones de zorro por el lince boreal (Lynx lynx) en Suecia (Helldin
et al. 2006), o la limitación de meloncillos (Herpestes ichneumon) por el lince ibérico
en España (Palomares et al 1995). De esta forma la regresión de las poblaciones de lince
ibérico en el siglo pasado (Rodríguez y Delibes 2003) probablemente haya contribuido
al aumento de la abundancia y distribución de algunos carnívoros generalistas de
tamaño medio como el observado recientemente para el meloncillo (Recio y Virgós
2010). Existen también ejemplos en aves como el descrito en Alemania para el búho
real y dos rapaces de tamaño medio como el azor (Accipiter gentilis) y el busardo
ratonero (Buteo buteo) (Chacarov y Krüger 2010).
La fragmentación y degradación de hábitats debido al creciente desarrollo de diferentes
actividades humanas (p. ej. agricultura, explotación maderera, infraestructuras, etc.) han
sido reconocidas entre los factores con mayor impacto sobre la biodiversidad (Sala et al.
2000). Aparte de la anteriormente citada disminución de depredadores apicales, la
transformación de algunos hábitats ha facilitado el incremento de recursos alimentarios
10
para muchos depredadores generalistas, como por ejemplo diferentes especies de
roedores (Thirgood et al. 2000b; Šálek et al. 2010; Luque-Larena et al. 2013). Thirgood
y colaboradores (2000b), por ejemplo, mostraron cómo en Escocia los aguiluchos
pálidos (Circus cyaneus) se beneficiaron del incremento en la abundancia de pequeños
roedores debido al aclarado de los brezales por el pastoreo, lo que supuso el incremento
de depredación incidental sobre el lagópodo escocés (Lagopus lagopus scoticus). La
actividad agrícola también puede incrementar la abundancia de ciertas presas
consumidas habitualmente por numerosos depredadores generalistas, como son algunos
micromamíferos (Luque-Larena et al. 2013) o el caso de algunos invertebrados y
pequeñas aves, asociados a los linderos entre cultivos (Vickery et al. 2002). Igualmente
los productos derivados de los cultivos agrícolas también pueden beneficiar a ciertos
depredadores generalistas omnívoros que incluyen de forma frecuente alimentos como
frutos y semillas en su alimentación. Este es el caso de algunos carnívoros de tamaño
medio y algunos córvidos (Soler et al. 1993; Rosalino y Santos-Reis 2009).
Por otro lado en ambientes fuertemente antropizados la actividad humana genera un
importante volumen de desperdicios (p. ej. basureros, merenderos, restos de granjas,
etc) que son fuente de alimentación suplementaria para muchos de estos depredadores
generalistas. De esta forma se ha observado cómo los zorros que habitan las periferias
de pueblos en entornos rurales, o incluso en las grandes ciudades, incluyen en su dieta
una importante proporción de alimentos de origen antrópico como basura o carroña de
ganado (Contesse et al. 2004; Webbon et al. 2006). Esta fuente de alimentación puede
suponer un aumento de la supervivencia y, por tanto, de la abundancia de las
poblaciones de zorros en estos ambientes (Bino et al. 2010). De forma similar algunos
córvidos también pueden verse beneficiados por estas fuentes de alimentación
antrópicas. Por ejemplo, se ha observado cómo la reducción de alimento subsidiario tras
el cierre de varias piscifactorías provocó una reducción de la densidad de nidos de
urraca (Pica pica) en una región de Norteamérica (Stone y Trost 1991). Más
recientemente se ha señalado que una alta disponibilidad de alimento de origen
antrópico puede favorecer la reproducción, supervivencia de adultos y abundancia local
de diferentes especies de córvidos (Marzluff y Neatherlin 2006).
11
Ecología del zorro y la urraca: paradigma de especies generalistas
El zorro y la urraca representan el paradigma de especies generalistas debido a su gran
flexibilidad ecológica en cuanto a requerimientos de hábitat, alimentación, parámetros
reproductivos y capacidad de adaptación a los cambios en el medio, como los
producidos por la actividad humana. Por todo ello, pueden llegar a alcanzar elevadas
abundancias (Birkhead 1991; Sillero-Zubiri et al. 2004).
El zorro es el carnívoro de tamaño medio más abundante y ampliamente distribuido en
todo el mundo. Especie de distribución holártica, se encuentra en grandes áreas del
Paleártico, incluida la Península Ibérica (Blanco 1998; Sillero-Zubiri et al. 2004). No
presenta requerimientos específicos de hábitat, estando presente tanto en ambientes
naturales como en ambientes fuertemente antropizados e incluso en el centro de grandes
ciudades (Contesse et al. 2004; Sillero-Zubiri et al. 2004; Webbon et al. 2006). Se
considera un depredador oportunista y omnívoro, que incluye en su dieta alimentos
vegetales, animales y desperdicios de origen antrópico (Díaz-Ruiz et al. 2013). Presenta
respuestas funcionales ante la disminución en la disponibilidad de su principal fuente de
alimento en cada situación, adaptándose al consumo de otros alimentos secundarios
(Ferreras et al. 2011). Se trata de una especie monoestra, es decir, que solo tiene un
ciclo reproductor al año (Voigt y Macdonald 1984), presentando una alta tasa de
reproducción, con tamaños de camada variables en función de los recursos disponibles,
que oscilan entre 1 y 12 cachorros (López-Martín 2010). El zorro dispone de
mecanismos de reproducción compensatoria, aumentando su productividad en
situaciones de alta mortalidad (Heydon y Reynolds 2000). Por lo general, una parte
importante de su población está compuesta por individuos no reproductores sin
territorios definidos, por lo que el proceso de recolonización de territorios vacíos puede
ser rápido cuando hay una mortalidad alta de adultos territoriales (Reynolds et al. 1993;
Cavallini 1996).
La urraca también es una especie ampliamente distribuida y abundante en muchas zonas
de Asia, el oeste de Norteamérica y Europa, incluida la Península Ibérica (Birkhead
1991; Martínez 2011). Aunque se encuentra en diferentes tipos de hábitats, que van
desde áreas naturales a zonas urbanas, suele alcanzar las mayores densidades en
ambientes agrícolas humanizados (Martínez 2011). La urraca es un generalista
omnívoro en cuanto a sus hábitos alimentarios que consume un amplio espectro de
12
alimentos de origen vegetal y animal, pudiendo beneficiarse a su vez de recursos
alimenticos de origen antrópico (Birkhead 1991). A diferencia del zorro, su papel como
depredador de aves, tanto protegidas como cinegéticas, no está claro, aunque algunos
trabajos indican que puede consumir huevos, pollos e incluso adultos de algunas
especies de estas aves (Groom 1993; Herranz 2000; Fernández-Juricic et al. 2004; Roos
y Pärt 2004). Presentan un solo ciclo reproductor al año, y una alta tasa de reproducción,
con puestas de entre 4 y 10 huevos (Birkhead 1991; Martínez 2011). En caso de pérdida
de la puesta pueden efectuar una puesta de sustitución como mecanismo de
compensación de pérdidas en la población (Pónz y Gil-Delgado 2004). Una parte
importante de sus poblaciones está formada por individuos no reproductores que pueden
reemplazar rápidamente cualquier pérdida de algún miembro de las parejas
reproductoras, y completar de forma exitosa la reproducción (Birkhead 1991).
Tanto zorro como urraca están considerados por algunos sectores de la sociedad como
especies perjudiciales para diferentes intereses humanos, como la agricultura, la
actividad cinegética o la ganadería, en prácticamente todo su rango de distribución; lo
cual hace que a menudo sean objeto de control (Birkhead 1991; Sillero-Zubiri et al.
2004).
El control de depredadores como herramienta de gestión y conservación Actualmente los impactos de los depredadores sobre algunos intereses humanos se
gestionan de forma diferente según el grado de protección de los mismos. De esta
forma, los impactos o daños generados por especies amenazadas suelen gestionarse a
través de compensaciones y subvenciones a los afectados o mediante translocaciones de
individuos, evitando la eliminación legal de los depredadores amenazados. Este tipo de
gestión está normalmente asociado a los daños producidos al ganado por grandes
depredadores como los lobos (pagos de indemnizaciones; aunque en algunas zonas
también se autoriza su caza), o que pueden afectar a la integridad física de las personas
como es el caso de los grandes felinos en algunas zonas (translocaciones de individuos
conflictivos) (Boitiani et al. 2010; Goodrich et al. 2011; Treves y Bruskotter, 2014).
En cambio, el control letal de depredadores es una medida habitual de gestión de la
depredación causada por depredadores generalistas abundantes (Treves y Naughton-
Treves 2005). Se utiliza como herramienta de gestión en la conservación de ecosistemas
y especies amenazadas, como medida sanitaria para el control de zoonosis, como
13
protección del ganado o en la gestión cinegética (Prught et al. 2009; Beja et al. 2009;
Saunders et al. 2010; Baesley et al. 2013). El control de depredadores introducidos, por
ejemplo, es una herramienta utilizada a menudo en acciones de conservación en zonas
donde estas especies han causado un gran impacto ecológico o pueden llegar a hacerlo.
Un claro ejemplo es el control de las poblaciones de zorro en Australia, donde el cánido
ha contribuido a la extinción de varias especies de vertebrados autóctonos,
representando un grave problema para la conservación de la fauna nativa (Saunders et
al. 2010). Igualmente el control de gatos domésticos asilvestrados (Felis catus) es una
acción de gestión habitual para la recuperación de fauna en numerosas islas de todo el
mundo, ya que su depredación ha contribuido al declive poblacional e incluso extinción
de numerosas especies (Medina et al. 2011).
La eliminación de algunos depredadores generalistas que actúan como reservorios de
enfermedades ha sido una herramienta empleada para el control y erradicación de
algunas zoonosis. Algunos ejemplos son el control poblacional de tejones (Meles meles)
empleado en Reino Unido para minimizar el riesgo de trasmisión de la tuberculosis
bovina (Smith et al. 2001; Bielby et al. 2014), el control de las poblaciones de zorros
para limitar el avance de la rabia en gran parte de Europa (Holmala y Kauhala 2006) o
el control de mapaches (Procyon lotor) en Norteamérica por ser reservorio de estas y
otras enfermedades infecciosas (Baesley et al. 2013). Sin embargo, el control de
depredadores generalistas por motivos de conservación y sanidad, solo se realiza en
casos excepcionales y bajo un estricto seguimiento por parte de la administración.
Por el contrario, el control de depredadores generalistas con fines cinegéticos es una
medida ampliamente extendida en diferentes zonas de todo el mundo (Reynolds y
Tapper 1996) debido a que los cazadores lo consideran con frecuencia fundamental para
aumentar la abundancia de las especies cinegéticas (Delibes-Mateos et al. 2013; Ljung
et al. 2014). Aunque en algunas zonas se controlan grandes depredadores para fomentar
especies de caza mayor (Musiani y Paquet 2004), el control orientado a depredadores de
pequeña o mediana talla, para el fomento de especies de caza menor, es probablemente
mucho más común y extendido. En Reino Unido, por ejemplo, es muy común el control
de zorros, tejones, pequeños mustélidos y córvidos como la urraca y la corneja negra
(Corvus corone) para fomentar las poblaciones de aves cinegéticas como la perdiz gris
(Perdix perdix) o los lagópodos (Tapper et al. 1996, Thirgood et al. 2000a). En Francia
el trampeo de pequeños y medianos carnívoros como zorros, garduñas (Martes foina) y
14
martas (Martes martes) es una práctica habitual (Ruette et al. 2003). También se
controla la urraca de forma sistemática en gran parte del país al considerarse una especie
dañina para la caza (Chiron et al. 2013). Igualmente en Suecia el control de zorros,
tejones y urracas es una medida muy extendida para fomentar las poblaciones de varias
especies de caza menor como los lagópodos y las liebres (Lepus sp.) (Ljung et al. 2014).
En Portugal el control legal de zorros, meloncillos y urracas es una medida muy
empleada para fomentar las poblaciones de perdiz roja (Alectoris rufa), conejo de monte
(Oryctolagus cuniculus) y liebre ibérica (Lepus granatensis) (Beja et al. 2009).
Efectos derivados del control de depredadores Los diferentes efectos derivados del control de depredadores son uno de los principales
puntos de controversia que genera esta actividad. Esto es debido en parte a la falta de
conocimiento científico, pero también a que los resultados obtenidos en los trabajos que
han estudiado estos efectos son a menudo contrapuestos o poco concluyentes. Como se
ha indicado anteriormente, con el control de depredadores se pretende un efecto
beneficioso sobre las presas que se quieren fomentar. Sin embargo, por lo general no se
consideran los efectos sobre especies no relacionadas directamente con el control. En
este sentido podríamos agrupar los efectos derivados del control de depredadores en tres
categorías: 1) Efecto sobre las presas que se pretenden fomentar, 2) Efecto sobre los
depredadores objeto del control y 3) Efecto sobre otras especies que no son objeto de
control.
Efecto sobre las presas
Existe gran controversia en cuanto a la efectividad del control de depredadores para
fomentar las poblaciones de ciertas presas. Por un lado, diversos trabajos no encuentran
un efecto significativo del control de depredadores sobre el incremento de las presas
(Kauhala et al. 2000; Keedwell et al. 2002). Por ejemplo, el control de múltiples
depredadores durante 20 años en una zona de Nueva Zelanda provocó cierto efecto
positivo a corto plazo en las poblaciones de kaki (Himantopus novaezelandiae), un ave
amenazada, pero dicho efecto desapareció posteriormente pese a mantener el control
(Keedwell et al. 2002). Por el contrario, varias revisiones indican que el control de
depredadores puede producir mejoras en las poblaciones de presas bajo ciertas
condiciones (Holt et al. 2008; Salo et al. 2010; Smith et al. 2010). Estas revisiones
coinciden en señalar que la eficacia del control depende de varios factores como la
15
duración e intensidad de las extracciones, el número de especies de depredadores
controlados, el tipo de depredador (autóctono o exótico), el tipo de presa que se intenta
recuperar, etc. Estos trabajos también señalan la importancia de los métodos de
seguimiento de las poblaciones de presas como algo fundamental para poder determinar
los efectos del control de sus depredadores.
Efecto sobre los depredadores generalistas objeto de control
La mayor parte de trabajos científicos existentes sobre control de depredadores evalúan
el efecto que éste tiene sobre las poblaciones de presas que se pretende fomentar (ver
apartado anterior), mientras que pocos evalúan el efecto sobre las poblaciones de la
especie objeto del control. Normalmente se asume que la extracción de un número de
animales conlleva una reducción del tamaño de la población. Sin embargo, no siempre
es así debido a que algunas especies que se pretenden controlar, como los depredadores
generalistas, presentan mecanismos para compensar reducciones en sus poblaciones. El
zorro y la urraca son un claro ejemplo en ese sentido, como se ha señalado
anteriormente.
Una parte importante de las poblaciones de zorro y urraca está constituida por
individuos no reproductores que contribuyen a la rápida respuesta demográfica frente a
actuaciones de control (Birkhead 1991; Cavallini 1996). Se ha descrito que una
eliminación de individuos adultos territoriales, sin reducir la disponibilidad de alimento,
va seguida de la ocupación de los territorios vacíos por individuos flotantes (Reynolds
et al. 1993; Chiron y Juliard 2013). Además de la rápida ocupación de territorios, las
poblaciones de estos depredadores pueden responder a la extracción con mecanismos de
reproducción compensatoria, aumentando la productividad (Heydon y Reynolds 2000) o
haciendo puestas de reposición (Pónz y Gil-Delgado 2004).
Varios trabajos han puesto de manifiesto la dificultad de reducir las poblaciones de
zorro, incluso empleando métodos de control masivos como cebos envenenados
específicos (Saunders et al. 2010). A menudo el control sólo es eficaz a corto plazo
(Harding et al. 2001), y en algunos casos ineficaz para reducir las densidades (Baker y
Harris 2006). Por el contrario, en un estudio observacional realizado a gran escala en
Inglaterra se comprobó que el control de zorros mediante distintos métodos puede
reducir sustancialmente la abundancia de este carnívoro en un amplio rango de
circunstancias (Heydon y Reynolds 2000). En cualquier caso, la evaluación
16
experimental de la efectividad de los métodos de captura de zorros para reducir sus
poblaciones es complicada, debido en parte a la dificultad de realizar estimas fiables de
su abundancia. Estas suelen requerir en el caso de los carnívoros metodologías costosas
y sofisticadas (Heydon et al. 2000; Schauster et al. 2002).
La efectividad del control de depredadores para reducir la densidad de urracas ha sido
menos estudiada que en el caso del zorro. No obstante, diferentes trabajos encuentran
como el control de urracas puede ser efectivo en la reducción de sus poblaciones a
escala local y regional (Stoate y Szuczur 2001, 2005; Chiron y Julliard 2007).
Recientemente se ha descrito cómo el control intensivo de urracas continuado en el
espacio y en el tiempo propiciaba el descenso de las poblaciones así como la
desestructuración de la población reproductora, que estaba dominada por individuos
jóvenes en zonas donde el control era más intensivo (Chiron y Julliard 2013).
Aparte de los efectos sobre la abundancia y la dinámica poblacional de la especie
controlada, las extracciones realizadas mediante el control de depredadores también
puede tener efectos a nivel comportamental cuando este es una importante causa de
mortalidad para la especie. En Australia, por ejemplo, se ha observado como los dingos
modifican sus ritmos de actividad diarios de acuerdo a si sus poblaciones son o no
controladas; son más nocturnos en zonas con que en zonas sin control (Brook et al.
2012).
Efecto sobre especies que no son objeto de control
El control de depredadores puede tener efectos negativos sobre otras especies que no
son objeto del control, tanto cuando el control es selectivo, es decir, solo se extrae la
especie objeto de control, como cuando no lo es, extrayéndose también otras especies.
La hipótesis de la liberación de competidores (del inglés “Competitor Release
Hypothesis”) propone como la eliminación de una especie dominante dentro de una
comunidad puede ser aprovechada por otra especie subordinada que, ante la falta de su
competidor, incrementa su abundancia (Caut et al. 2007). Aunque esta hipótesis se basa
en una aproximación teórica realizada para una comunidad de roedores sometida a
control, este efecto puede darse también en las comunidades de depredadores como por
ejemplo en los mesocarnívoros (Barrull et al. 2014). Cuando el control es selectivo se
puede producir un aumento de otros depredadores subordinados. En Reino Unido, por
ejemplo, se observó cómo, tras el control selectivo de un depredador dominante como el
17
tejón, realizado para frenar la expansión de la tuberculosis, la abundancia de zorros
(competidor subordinado) incrementó (Trewby et al. 2008).
Sin embargo, el control de depredadores desarrollado en algunas fincas de caza no es
selectivo y se eliminan ilegalmente especies de mesocarnívoros, que a priori no son
objeto de control (Duarte y Vargas 2001; Barrull et al. 2011). Estudios recientes
basados en modelos teóricos de simulación han puesto de manifiesto que diferentes
niveles de control no selectivo de las poblaciones de zorros podrían alterar las
comunidades de carnívoros con un aumento en la abundancia de la especie objetivo, es
decir el zorro. Por el contrario, las poblaciones de otras especies no objetivo
(competidores del zorro) como el tejón, la garduña y la marta (Martes martes) podrían
reducirse notablemente o incluso desaparecer debido a las menores tasas reproductivas
de estas especies (Casanovas et al. 2012; Lozano et al. 2013).
Pero el control de depredadores no solo puede tener efectos sobre otros depredadores
que a priori no son objeto de control sino que puede afectar de forma indirecta a otras
especies no relacionadas directamente con el control. El control intensivo de
depredadores puede perjudicar a la diversidad y estructuración de algunos grupos de
presas secundarias, como se ha comprobado en Norteamérica para el control de coyotes
y las comunidades de micromamíferos (Henke y Bryant 1999). En dicho estudio se
observó que en zonas de baja abundancia de coyote debido a su intenso control, las
comunidades de roedores eran menos diversas y estaban dominadas por pocas especies
que se libraron de la depredación de los coyotes, y desplazaron por competición a otras
especies de la comunidad. Otro ejemplo del posible efecto indirecto del control de
depredadores sobre otras especies sería el del control de urracas y el críalo (Clamator
glandarius). El críalo es un ave parásita de los nidos de urraca que en gran medida
depende de ésta para completar su ciclo reproductor (Martínez 2011; Soler 2012). Por lo
tanto, tanto el críalo como otras aves que utilizan para criar los nidos abandonados de
urraca, podrían verse perjudicados cuando éstos son destruidos como medida de control
(Birkhead 1991).
Además, la extracción intensa de estos depredadores generalistas puede tener efectos
sobre diferentes procesos ecológicos en los que estas especies desempeñan diferentes
funciones. Por ejemplo el zorro es un importante dispersor de semillas de ciertas plantas
y también puede regular las poblaciones de ciertas presas consideradas como plaga por
18
el hombre (Hanski et al. 1991; Fedriani y Delibes 2009). Igualmente la urraca juega un
papel de control biológico sobre ciertos grupos de invertebrados potencialmente
perjudiciales para los cultivos (Birkhead 1991).
El control de depredadores en España En España el control de depredadores es una práctica bastante extendida que se usa
tanto como parte de la gestión cinegética como para la conservación de ecosistemas y
especies amenazadas. En relación al segundo de los casos, existen varios ejemplos de
control de depredadores introducidos, como el visón americano (Neovison vison) por su
impacto sobre diferentes presas así como por ser competidor del autóctono y amenazado
visón europeo (Mustela lutreola) (Zuberogoitia et al. 2010). Más reciente es el control
de mapaches, el cual ha colonizado varias zonas de España a partir de las liberaciones
de particulares, y tiene un gran potencial como depredador, como competidor de otros
depredadores autóctonos y como reservorio de enfermedades (García et al. 2012).
Aparte del control de depredadores exóticos, en España también se han controlado
depredadores autóctonos como medida para la conservación de especies amenazadas.
Por ejemplo, en los Pirineos se han controlado zorros y translocado otros
mesocarnívoros generalistas para la protección del urogallo (Tetrao urogallus)
(Fernández-Olalla 2011). Sin embargo, el control de depredadores generalistas por
motivos de conservación se realiza en España de forma puntual, en casos excepcionales
y bajo un estricto seguimiento por parte de la administración, siendo el control ligado a
la gestión cinegética mucho más común y extendido a lo largo de gran parte del país.
La caza menor es un recurso económico importante en muchas áreas rurales de España
(Bernabeu, 2000). Las principales especies de caza menor son la perdiz roja, el conejo
de monte y la liebre. En las últimas décadas la abundancia de las poblaciones silvestres
de estas especies ha sufrido una importante disminución en gran parte de la Península
Ibérica, siendo más acusada en la perdiz roja y el conejo (Blanco-Aguiar et al. 2003;
Blanco-Aguiar 2007; Delibes-Mateos et al. 2009). Esto parece haber provocado un
incremento en el uso de métodos para el control de depredadores (tanto legales como el
ilegales) con la intención de recuperar estas especies (Villafuerte et al. 1998; Márquez et
al. 2012). Al igual que lo descrito anteriormente, en España el control de depredadores
es una medida muy extendida en gran parte de los cotos de caza, principalmente de caza
19
menor, como así lo confirman varios estudios (Tabla 1). El zorro y la urraca son las
especies en las que se suele centrar este control (Tabla 1) (Díaz-Ruiz y Ferreras 2013).
Tabla 1. Trabajos que han estudiado la extensión del uso del control de depredadores en
España como herramienta de gestión cinegética. N es el tamaño muestral de cada trabajo. a
porcentaje de provincias en las que el control se realiza con una intensidad media-alta; el resto
de los encuestados reconoció un baja intensidad en el control de depredadores. b Información no
disponible. c porcentaje de los cotos que realizan control en los que se realiza sobre cada especie
o grupo de especies
Referencia Zona de
estudio Datos
Tipo de
Áreas N Control Zorro Córvidos
Angulo 2003 Andalucía
Entrevistas
personales con los
gestores de los cotos
95%Cotos
de caza
menor-
mayor
5% áreas
protegidas
307 48% - b - b
Piorno 2006 España
Peninsular
Encuestas a técnicos
de caza de las
Administraciones
Provinciales
Cotos de
caza
menor-
mayor
47 66%a - b - b
Delibes-Mateos
2008 Centro-Sur
Entrevistas
personales con
Cazadores-Gestores
Cotos de
caza
menor-
mayor
60 70% 95%c 5% c
Rios-Saldaña
2010
Castilla-La
Mancha
Planes técnicos de
caza
Cotos de
caza
menor-
mayor
5365 94.4% 82% c 56% c
Delibes-Mateos
et al. 2013 Centro
Entrevistas
personales con los
gestores de los cotos
Cotos de
caza menor 59 90% 85% c 80% c
20
A pesar de tratarse de una actividad legal y regulada, el control de depredadores, y
especialmente el desarrollado en la gestión cinegética, es una actividad que genera gran
controversia en la sociedad española con posicionamientos opuestos entre diferentes
grupos sociales: ecologistas, conservacionistas, científicos, administración, cazadores y
ganaderos (Herranz 2000; Lozano et al. 2006; Virgós et al. 2010). Esto es debido, al
menos en parte, a la poca información disponible sobre diferentes aspectos relacionados
con esta actividad, como son la idoneidad de los métodos de control empleados así
como los efectos derivados del control de depredadores (Díaz-Ruiz y Ferreras 2013).
Regulación legal del control de depredadores
Actualmente el control de depredadores en España está regulado por cuatro
ordenamientos: el internacional, el comunitario, el estatal y el autonómico, a través de
diferentes normativas (Tabla 2). La mayor parte de estas normativas se refieren a los
métodos de control, prohibiendo de forma general aquellos masivos y/o no selectivos, e
incluyen anexos donde se enumeran los diferentes métodos que quedan completamente
prohibidos, como por ejemplo el uso de cebos envenenados (p. ej. Convenio de Berna
1979) o el de cepos (Reglamento (CEE) nº 3254/91 de 1991). Estas normativas
coinciden en dejar una vía de excepción a la norma general, merced a la cual se pueden
autorizar determinados métodos bajo unos supuestos que justifiquen su uso (entre ellos
daños a la fauna).
Las diferentes normativas autonómicas vigentes en España son las que establecen las
especies que pueden ser objeto de control (Gálvez 2004). Por lo general solamente se
permite el control de ciertos depredadores generalistas, que en su mayoría están
catalogados como especies cinegéticas. En concreto, y salvo algunas excepciones según
cada región, se permite controlar cuatro especies silvestres: el zorro, la urraca, la grajilla
(Corvus monedula) y la corneja negra. También se suele permitir de forma excepcional
el control de otras dos especies de depredadores domésticos asilvestrados: el gato y el
perro (Canis lupus familiaris). Generalmente los depredadores cinegéticos pueden ser
cazados con armas de fuego durante la época hábil de caza. Además, se permite el uso
excepcional de otros métodos de captura fuera de la temporada cinegética para controlar
tanto estas dos especies domésticas como las cinegéticas. Los permisos de control
excepcional son concedidos por la administración regional según diferentes criterios,
que no siempre son los establecidos en estas normativas (Bernard 2008).
21
Tabla 2. Normativas vigentes en España sobre control de depredadores.
Nivel
Legislativo Normativas vigentes
Internacional
- Convención sobre la conservación de la vida silvestre y el medio
natural de Europa (“Convenio de Berna”. Berna, 19-IX-1979)
- Acuerdo entre la Unión Europea, Canadá y la Federación Rusa sobre
métodos de captura no cruel (Decisión 98/142/CE del Consejo de 26 de
Enero de 1998)
- Acuerdo ente la Unión Europea y los Estados Unidos de América sobre
métodos de captura no cruel (Decisión 98/487/CE de 13 de Julio de
1998)
Unión Europea
- Directiva 79/409/CEE, relativa a la conservación de las aves silvestres
(“Directiva de Aves”).
- Directiva 92/43/CEE relativa a la conservación de los Hábitats naturales
y de la fauna y flora silvestres (“Directiva Hábitats”).
- Reglamento (CEE) nº 3254/91 del Consejo, de 4 de noviembre de 1991,
por el que se prohíbe el uso de cepos en la Comunidad
- Reglamento (CE) nº 1771/94 de la Comisión, de 19 de julio de 1994,
sobre comercialización de pieles de animales salvajes
- Reglamento (CE) nº 35/97 de la Comisión de 10 de enero de 1997,
sobre la certificación de pieles
- 97/602/CE: Decisión del Consejo de 22 de julio de 1997
Estatal
- Ley 42/2007 de Conservación del Patrimonio Natural y de la
Biodiversidad. Título III. Capítulo IV – De la protección de las especies
en relación con la caza y la pesca continental
- Directrices técnicas para la captura de especies cinegéticas predadoras:
homologación de métodos de captura y acreditación de usuarios.
Aprobadas por la Conferencia Sectorial de Medio Ambiente. 13 de julio
de 2011
Autonómica - Leyes y Reglamentos Autonómicos de Ordenación de la Caza
Métodos de control de depredadores generalistas
Uno de los principales motivos de controversia en relación al control de depredadores es
la efectividad y selectividad de los métodos utilizados. Por lo general los cazadores
consideran que los métodos permitidos por la legislación vigente son pocos eficaces
22
para controlar a los depredadores (Delibes-Mateos et al. 2013). En los últimos años
algunas comunidades autónomas han iniciado el proceso legal de homologación de
determinados métodos de control de depredadores generalistas basándose en ensayos de
campo, en sendos acuerdos internacionales sobre métodos de captura no cruel (Ver
Tabla 2), y en una Norma ISO (International Organization for Standardization 1999)
sobre evaluación de métodos de captura y retención de mamíferos (Díaz-Ruiz y Ferreras
2013).
Como se ha señalado anteriormente, el zorro y la urraca son las dos principales especies
en las que se centra el control de depredadores en España. En este sentido, actualmente
los principales métodos de captura utilizados con carácter excepcional para el control
poblacional de estas especies son los lazos y jaulas-trampa para la captura de zorros y
jaulas-trampa para la captura de urracas (Delibes-Mateos et al. 2013). Diferentes
trabajos han evaluado de forma empírica la eficiencia de captura de las especies
objetivo, la selectividad y los daños relacionados con la captura de varios de estos
métodos utilizados habitualmente para controlar zorros y urracas en España (Díaz-Ruiz
et al. 2013).
Recientemente se ha aprobado un documento, consensuado entre las administraciones
central y autonómicas, que recoge las directrices para establecer qué métodos pueden
homologarse para realizar control de depredadores (Conferencia Sectorial de Medio
Ambiente 2011). Sin embargo, la citada Norma ISO y su interpretación han suscitado
controversia y críticas entre científicos que la consideran insuficiente e incluso errónea
en algunos de sus planteamientos, tanto en lo relativo a bienestar animal como en
algunos conceptos aplicados a los dispositivos de captura (Iossa et al. 2007; Virgós et
al. 2010).
Métodos para el control de zorros
Las jaulas-trampa para zorros consisten en un compartimento de captura con una o dos
puertas de entrada, que se cierran mediante un balancín al ser pisado por el animal, y un
compartimento opcional para el cebo (Fig. 1). Pueden utilizarse con cebo vivo o muerto
(Ferreras et al. 2003; 2007; Muñoz-Igualada et al. 2008). Tanto los lazos tradicionales
actuales como dos versiones norteamericanas más complejas (“Lazo Americano” y
“Lazo Wisconsin”) consisten en un cable de acero en el que en uno de sus extremos
presenta un lazo corredizo con un tope (salvo en el modelo “sin tope”) para que este no
23
se cierre totalmente sobre el cuello del animal, fijándose el otro extremo al terreno para
retener al animal capturado (Muñoz-Igualada et al. 2010). En España se han evaluado
también dos nuevos sistemas diseñados en Estados Unidos para la captura de cánidos,
las trampas Belisle y Collarum (Shivik et al. 2000). Las trampas Belisle (Edouard
Belisle, Saint Veronique, PQ, Canadá) consisten en un lazo de acero propulsado que
retiene al animal por la extremidad al accionar una pletina central de disparo (Shivik et
al. 2000; Muñoz-Igualada et al. 2008). La trampa Collarum (Wildlife Control Supplies,
East Granby, CT, USA) es también un lazo de acero propulsado que retiene al animal
por el cuello (Shivik et al. 2000; Ferreras et al. 2007; Muñoz-Igualada et al. 2008). En
este último caso, el sistema de disparo precisa de una respuesta activa del animal ante
un atrayente oloroso. Ambos lazos propulsados se instalan enterrados, quedando tan
sólo visible en la superficie, en el caso del Collarum, el disparador con el atrayente
(Ferreras et al. 2007; Muñoz-Igualada et al. 2008).
Métodos para el control de urracas
Las jaulas-trampa para capturar urracas son el método más empleado para controlar
urracas en España ya que los cazadores las consideran eficaces para reducir las
abundancias del córvido (Delibes-Mateos et al. 2013). Por lo general estas trampas
tienen un compartimento central donde se coloca una urraca viva que actúa como
reclamo y una serie de compartimentos de captura (2 o 4) alrededor que se accionan de
forma independiente (Ferreras et al. 2007).
Efectos del control de depredadores en España
En España existen pocos trabajos que hayan estudiado los diferentes efectos del control
de depredadores. De esta forma la efectividad del control de depredadores para
fomentar las presas en España está poco clara. El único trabajo experimental de este tipo
realizado en España evaluó la efectividad del control selectivo de depredadores (zorro y
urraca) para mejorar la supervivencia de la perdiz roja (Mateo-Moriones et al. 2012). El
control de depredadores mejoró la supervivencia de los pollos, especialmente de
aquéllos de más de un mes de edad, pero no mejoró la supervivencia de los adultos ni de
los nidos, ni el tamaño de las poblaciones de perdiz. Herranz (2000) describe resultados
similares referidos al control de urracas en un coto de caza de Castilla-La Mancha,
donde tras el control se incrementó el tamaño de bando de las perdices pero no se
consiguió incrementar sus poblaciones ni las de paloma torcaz (Columba palumbus).
Del mismo modo, en un trabajo reciente realizado en el centro de España no se encontró
24
ninguna relación entre la intensidad de control de zorros y las densidades de perdiz roja
(Díaz-Fernández et al. 2013). Por el contrario, Delibes-Mateos et al. (2008c) hallaron
que el control de depredadores y el manejo de hábitat fueron las dos únicas medidas de
gestión relacionadas con la tasa de cambio en la abundancia de conejo en cotos de caza
del centro-sur de España entre 1993 y 2002. Igualmente, Virgós y Travaini (2005)
observaron mayores abundancias de conejo en cotos de caza con gestión cinegética
intensiva que en zonas donde no se realizaba este tipo de gestión.
Varios estudios han evaluado también la efectividad del control de depredadores para
incrementar especies de interés para la conservación en España. Por ejemplo, en un
experimento realizado en el Pirineo el control de zorro y las translocaciones de marta,
garduña y gato montés (Felis silvestris) no produjeron mejoras en el éxito reproductor
del urogallo en Pirineos (Fernández-Olalla 2011). Por el contrario, la declaración de un
área protegida en Almería, y la consiguiente prohibición de utilizar control de
depredadores, repercutió negativamente en las poblaciones de paseriformes esteparios
(Suárez et al. 1993). Estos resultados concuerdan con los obtenidos más recientemente
por Estrada et al. (2012), quienes observaron mayores densidades de ciertas aves
esteparias en cotos de caza donde se realizaba control de zorros. Por lo tanto, la
efectividad del control de depredadores para fomentar las presas en España está poco
clara.
El efecto de las extracciones sobre las poblaciones de los depredadores controlados
igualmente ha sido poco estudiado en España, encontrando resultados dispares. Así en
Doñana no se encontró ninguna respuesta poblacional clara a las extracciones de zorros
realizadas por personal del Parque Nacional durante cuatro años, probablemente debido
a una baja intensidad y gran variabilidad interanual de extracción (Palomares et al.
2010). Igualmente Virgós y Travaini (2005) no encontraron diferencias en la presencia
de zorros entre zonas cinegéticas (donde se asumía el uso de métodos de control de
depredadores) y zonas sin caza del centro de la Península Ibérica. En un experimento
realizado en Pirineos se consiguió reducir la densidad de zorros en una de las zonas de
estudio durante uno de los años de estudio. No obstante, esto no se consiguió en otras
dos zonas de trabajo ni en la misma zona durante los otros dos años que duró el estudio
(Fernández-Olalla 2011). De forma similar las extracciones experimentales realizadas
en dos localidades en Navarra redujeron la abundancia en una de las localidades de
25
estudio, mientras que este efecto no fue tan evidente en la otra localidad (Mateo-
Moriones et al. 2012).
Prácticamente no existen estudios que hayan evaluado experimentalmente el efecto de
las extracciones de urraca sobre sus poblaciones. Herranz (2000) observó una reducción
significativa de la población de urracas en un coto de caza tras una campaña de control
mediante destrucción de nidos y caza de adultos; sin embargo, no aportó información
sobre la evolución tras cesar el control. Un experimento realizado en Navarra, no pudo
evaluar el efecto de las extracciones sobre las poblaciones de urracas por ser éstas muy
poco abundantes (Mateo-Moriones et al. 2012).
Por último, en España no se ha estudiado de forma experimental el efecto del control de
depredadores sobre otras especies no relacionadas directamente con el control. Hasta la
fecha solamente un estudio observacional ha evaluado el efecto del control no selectivo
de zorros en otras especies de mesocarnívoros como el tejón y la garduña (Barrull et al.
2014). No existe ningún trabajo similar en el caso de las urracas ni estudios sobre el
efecto potencial del control de depredadores sobre el comportamiento de la especie
objetivo del control.
OBJETIVOS Y ESTRUCTURA DE LA TESIS Como queda patente en lo anteriormente dicho, el conocimiento científico en materia de
control de depredadores es escaso, especialmente en España (Díaz-Ruiz y Ferreras
2013). El objetivo principal de esta tesis es, por tanto, contribuir al conocimiento
científico sobre la gestión del zorro y la urraca, mediante el estudio de diferentes
aspectos relacionados como la ecología trófica de estas especies, la adecuación y mejora
de los métodos empleados para su control y las implicaciones ecológicas derivadas del
control de sus poblaciones. Esta tesis pretende aportar avances en el conocimiento
científico para mejorar la gestión de los depredadores generalistas y, por lo tanto, de las
especies que pueden verse afectadas por el control de dichos depredadores. Para la
consecución del objetivo principal, en esta tesis se plantean los siguientes objetivos
parciales:
1) Analizar la ecología trófica de las dos especies seleccionadas como modelo de
estudio, el zorro y la urraca, por ser la alimentación el principal motivo en el que se basa
el control de sus poblaciones. En el capítulo 1 se plantea un estudio de la alimentación
26
del zorro a escala biogeográfica de la Península Ibérica, una perspectiva espacial más
amplia a la descrita hasta ahora, para definir patrones de su alimentación que ayuden a
una mejor compresión de la flexibilidad trófica del cánido. El objetivo del capítulo 2 es
caracterizar la dieta de las urracas durante su época de reproducción en zonas agrícolas
del centro de España para determinar la frecuencia de consumo de ciertos alimentos
como huevos y aves, y estudiar la influencia de diferentes factores intrínsecos (sexo-
edad) y extrínsecos (localidad) en la composición de su alimentación.
2) Evaluar la efectividad y selectividad de los métodos de captura usados con mayor
frecuencia en España para controlar zorros y urracas. Además, se pretende analizar
diferentes formas de mejorar la efectividad y selectividad de estos métodos de captura.
En concreto se evalúa el uso combinado de diferentes cebos y atrayentes para mejorar la
eficiencia de captura y selectividad de las jaulas-trampa para zorros, así como la
evaluación de nuevos sistemas de captura alternativos como el sistema Collarum
(capítulo 3). Igualmente se evalúan las jaulas-trampas habitualmente empleadas para el
control de las poblaciones de urraca, ensayando diferentes variantes de uso con la
intención de mejorar este método de control (capítulo 4).
3) Analizar posibles efectos del control de depredadores sobre las especies objeto de
control así como sobre otras especies. Por un lado estudiar los efectos de las
extracciones de estos depredadores sobre la abundancia de sus poblaciones. En
concreto, estudiar el efecto a corto plazo de las extracciones experimentales de urracas
sobre sus poblaciones (capítulo 4). Por otro lado estudiar si el gradiente de intensidad de
control de depredadores está relacionado con la probabilidad de ocupación y detección
de depredadores objeto de control, como el zorro, y de otros que a priori no lo son,
como la garduña (capítulo 5). Por otro lado, se pretende evaluar si el control de zorros
tiene algún efecto sobre el comportamiento de esta especie (capítulo 6).
La Tesis está estructurada en 6 capítulos en formato de artículos científicos. Alguno de
ellos está publicado en revistas incluidas en el “Science Citation Index”, otros están
actualmente en revisión o en preparación para su publicación. Se incluye una discusión
general en la que se destacan los resultados más significativos obtenidos en los
diferentes capítulos de esta tesis. Finalmente se proponen futuras líneas de investigación
surgidas de este trabajo y las principales conclusiones obtenidas en cada capítulo.
27
CAPÍTULO 1: Biogeographical patterns in the diet of an opportunistic predator: the red fox Vulpes vulpes in the Iberian Peninsula
Díaz–Ruiz F, Delibes–Mateos M, García–Moreno JL, López–Martín JM, Ferreira C, Ferreras P (2013) Biogeographical patterns in the diet of an opportunistic predator, the red fox Vulpes vulpes in the Iberian Peninsula. Mammal Review 43: 59-70
28
Abstract Biogeographical diversity is central to the trophic ecology of predators. Understanding
the biogeographical trophic patterns of generalist predators, such as the red fox Vulpes
vulpes, is particularly challenging because of their wide distributions, broad trophic
spectra and high ecological plasticity, which often generate conflicts with humans. We
reviewed 55 studies from the Iberian Peninsula concerning the diet of the red fox to
describe its trophic patterns from a biogeographical perspective. We considered the
frequency of occurrence of seven food groups and characterized each study site
according to environmental variables. We tested relationships between geographical
variables and each food group independently, and assessed the consumption of
lagomorphs in relation to the other food groups. We also tested the relationships
between trophic diversity, the main food groups, latitude and altitude, and finally
investigated changes in the consumption of all food groups in relation to habitat type
and seasonality. We found a latitudinal pattern in the diet of the red fox, which was
characterized by a greater consumption of lagomorphs and invertebrates in southern
areas, and a higher intake of small mammals and fruits/seeds in northern regions.
Additionally, the consumption of invertebrates increased from east to west, while
fruit/seed consumption increased from west to east. Consumption of lagomorphs
decreased, and of small mammals increased, with altitude. Trophic diversity was not
associated with geographical variables. The intake of lagomorphs and small mammals
was greatest in Mediterranean scrub and forest, respectively. Reptiles and invertebrates
were consumed mostly during summer; fruits/seeds in autumn. Iberian red foxes show
variation in their feeding habits associated with environmental variables, which are in
turn associated with the availability of their main prey. Foxes select rabbits where they
are abundant, and feed on small mammals and fruits/seeds where lagomorphs are
scarce.
Keywords: carnivore, feeding patterns, generalist predator, Portugal, Spain
29
Introduction Feeding habits have been one of the most studied features of carnivore ecology. The
traditional approach to studies ofcarnivore diets is to investigate the feeding habits of
species (mainly in terms of diet composition) at local or regional scales (e.g. Brand et
al. 1976; Zapata et al. 2007; Wang and Macdonald 2009). Comprehensive studies of
carnivore trophic ecology at broader geographical scales have only recently been
undertaken (e.g. Clavero et al. 2003; Lozano et al. 2006; Zhou et al. 2011). The study of
trophic biogeographical patterns of predators is fundamental to understanding their
ecology and life history strategies (Daan and Tinbergen 1997). For instance, defining a
species as a trophic generalist or specialist is only relevant in the context of extensive
ecological studies in which variation in feeding behaviour among populations over a
broad range of environmental conditions is considered (Lozano et al. 2006).
Investigations of the diet of medium-sized carnivores at large biogeographical scales
have included studies of the Eurasian badger (Meles meles) (Roper and Mickevicius
1995; Goszczynski et al. 2000; Hounsome and Delahay 2005); the polecat (Mustela
putorius) (Lodé 1997); the common genet (Genetta genetta) (Virgós et al. 1999); the
Eurasian otter (Lutra lutra) (Clavero et al. 2003); the European wildcat (Felis silvestris)
(Lozano et al. 2006); and the Holarctic martens, (Martes sp.) (Zhou et al. 2011).
Surprisingly, this type of study is lacking for the red fox (Vulpes vulpes), which is the
world’s most widespread member of the order Carnivora (Sillero- Zubiri et al. 2004)
and one of the most abundant carnivore species in the Iberian Peninsula (Blanco 1998;
Palomo et al. 2007) and elsewhere.
Environmental and climatic conditions affect food availability, and can have an impact
on dietary composition and diversity (Hill and Dunbar 2002). Thus, variations in the
distribution of potential prey species across biogeographical regions have been
postulated to affect the feeding habits of medium-sized carnivores. For instance, dietary
diversity in wildcats increases at lower latitudes (i.e. Mediterranean areas; Lozano et al.
2006), where potential prey richness is greater (Rosenzweig 1995). Latitudinal gradients
have also been observed in relation to dietary diversity and in the consumption of
particular prey. For example, the Eurasian otter’s diet is more diverse in southern
localities, while further north the species is more piscivorous, predating upon a large
diversity of fish families (Clavero et al. 2003). Similarly, food availability can vary
along altitudinal gradients, and this can affect the dietary composition of carnivores. For
30
instance, small mammals (mice, voles and shrews) are the primary food of martens, but
are less frequently consumed at lower altitudes, where other food resources are more
abundant and are available throughout the year (Zhou et al. 2011).
Diet is one of the most studied aspects of the ecology of the red fox. Most studies
indicate that the red fox is a generalist predator that uses resources according to their
availability and hence is opportunistic in its behaviour (e.g. Webbon et al. 2006;
Dell’Arte et al. 2007). However, most studies were undertaken at local or regional
scales, and specific studies describing biogeographical patterns in the red fox diet are
lacking. Although some studies have shown variations in the feeding habits of foxes
based on environmental variables including habitat type (Fedriani 1996; Gortázar 1999),
the effects of latitude, longitude and altitude on the composition of fox diets at a larger
scale remain unknown. Similarly, there is a lack of information about how the
consumption by foxes of some preferred prey, such as lagomorphs or small mammals,
varies spatially at biogeographical scales.
The ecological features of red foxes can bring them into conflict with human activities
where their prey is of economic or conservation concern (Baker and Harris 2003). For
example, predation by foxes is often regarded as one of the factors preventing the
recovery of small game (Reynolds and Tapper 1995; Smedshaug et al. 1999; Beja et al.
2009; Knauer et al. 2010), and farmers consider predation of livestock by foxes to cause
economic losses (Moberly et al. 2004). Furthermore, several researchers have reported
negative impacts of fox predation on species of conservation concern (Yanes and Suárez
1996; Ruiz-Olmo et al. 2003; Dickman 2010). However, predators, including
generalists such as red foxes, play major roles in ecological processes by limiting
populations of pest species (O’Mahony et al. 1999; Newsome et al. 2001), reducing the
transmission of disease (Hudson et al. 1992; Millán et al. 2002) and acting as seed
dispersers (Guitián and Munilla 2010; Rosalino et al. 2010). Our ability to understand
biogeographical patterns is crucial for developing efficient management programs in the
context of human usage (Whittaker et al. 2005). From this perspective, a large-scale
study of the trophic ecology of the red fox could provide valuable knowledge
concerning its ecosystem functions and improve management of this predator.
The Iberian Peninsula is included in the Mediterranean Basin hotspot (Myers et al.
2000) and is thereby an interesting site for the study of biogeographical patterns (e.g.
31
Carvalho et al. 2011). It includes distinct Atlantic (Northern Iberia), Mediterranean
(Central and Southern Iberia) and Alpine (Pyrenees mountains) biogeographical regions
(Rivas-Martínez 1987; Figure 1.1.), and is characterized by high environmental
heterogeneity because of its climatic and physiographical complexity (the altitude
ranges from 0m at sea level to 3479m above sea level at Sierra Nevada, Granada,
Spain). The variability in environmental conditions underpins the diversity in
community composition and structure in this region (Blondel and Aronson 1999,
Stefanescu et al. 2004). Several patterns in the distribution and abundance of the main
prey species of Iberian predators have been described. For instance, wild rabbits
Oryctolagus cuniculus, which are a key prey for red foxes and other Iberian predators
(Delibes and Hiraldo 1981; Calzada 2000; Ferreras et al. 2011), are most abundant at
central–southern latitudes (Villafuerte et al. 1998), and small mammals show a gradient
in abundance and species richness from south to north (Soriguer et al. 2003). The theory
of feeding specialization predicts an increase in dietary diversity when the preferred
prey becomes scarce (Futuyma and Moreno 1988). In this study, we tested this
prediction in relation to the red fox and rabbits as its preferred prey. Although the
Iberian Peninsula is a relatively small biogeographical area, its high environmental
variability and biodiversity justifies a biogeographical analysis of the diet of resident
generalist carnivores such as the red fox.
Our main objective was to describe the trophic biogeographical patterns of the red fox
in the Iberian Peninsula, based on a comprehensive literature review. Specifically, we:
(i) evaluated changes in consumption by red foxes of main food groups in relation to
geographical variables (latitude, longitude and altitude); (ii) analysed the relationships
between red fox dietary diversity, consumption of its main prey and geographical
variables; (iii) assessed the relationships between the consumption of different food
groups and habitat type and season; and (iv) interpreted patterns in the diet of this
generalist predator from a biogeographical perspective.
32
Figure 1.1. Geographical distribution in the Iberian Peninsula of studies of the diet of the red
fox (Vulpes vulpes) included in this review. Biogeographical regions are shown, and the
numbers represent study site identifiers (ID; see Appendix 1.1.).
Material and Methods Literature compilation and standardization of dietary data
Various sources of information were used to review the available literature
comprehensively, as recommended by Pullin and Stewart (2006). Search engines (ISI
Web of Science and Google Scholar) were used to identify relevant scientific studies
containing information about the trophic ecology of the red fox in the Iberian
Peninsula.We searched for terms that were identified using the following combinations
of keywords: ‘red fox’ or ‘Vulpes vulpes’ and ‘diet’ or ‘feeding’ and ‘Iberian
Peninsula’, ‘Spain’ or ‘Portugal’. We consulted several zoological bibliographical data
bases including the Zoological Record (http://scientific.thomson.com/products/zr/) and
the bibliographical data set of the Spanish Society for the Conservation and Study of
Mammals (http://www.secem.es/Secem_la_biblioteca.htm). We also sought information
on the topic from informal contacts with expert researchers (colleagues working in
33
different institutions – universities and environmental public administration – in Spain
and Portugal). This provided us with less readily accessible sources of information,
including unpublished or unedited studies (e.g. PhD theses, MSc and BSc dissertations,
and public administration data bases).
We compiled a total of 55 published and unpublished studies concerning the diet of the
red fox in Portugal and Spain, spanning the period 1971–2008. Some authors reported
data pooled annually, others reported data pooled seasonally, and several provided both
annual and seasonal data. To simplify the statistical procedures, two independent data
bases were created for analysis: one comprising annual data and the other seasonal data.
These data bases were analysed independently (see Statistical analyses).
To standardize data from different geographical areas (for later comparison and
analysis), we excluded studies: (i) with small sample sizes (scat or stomachs; n < 30 for
anual studies and n < 15 for seasonal studies); (ii) reporting data for only one prey
group; (iii) containing duplicated information, e.g. academic dissertations later
published as scientific articles; and (iv) reporting only relative frequency of occurrence
(RF, expressed as the percentage of times one food ítem occurs in relation to the total
times all food items occur) or percentage biomass. This last exclusion meant that we
only considered studies reporting the frequency of occurrence (FO, expressed as the
percentage of scats/stomachs containing a particular food item) for the various food
groups. RF values are considered to be highly suitable for interpopulation comparisons
in diet studies (Clavero et al. 2003), and biomass is considered a direct measure of the
energetic value of prey items consumed (Reynolds and Aebischer 1991), and therefore
the best approximation to the true diet (Klare et al. 2011). However, only a small
proportion of the reviewed studies presented RF or biomass information, while FO is
widely used in carnivore diet studies and was used in most of the red fox studies
considered in this review. Moreover, FO can be used to assess whether a predator
behaves as an opportunist or as a specialist forager (Klare et al. 2011), and it is
considered a valid parameter for comparative purposes (Reynolds and Aebischer 1991;
Klare et al. 2011).
The application of the four exclusion criteria above resulted in a final set of 37 studies
that were further analysed to describe red fox feeding patterns in the Iberian Peninsula.
These studies were carried out in 39 locations distributed throughout the region (Figure.
34
1; for more detailed information, see Appendices 1.1. and 1.2.). The data were highly
heterogeneous among the variables, which reflected the diversity of environmental
conditions in the Iberian Peninsula. For example, a broad altitudinal range (20– 1425m)
was included, and various habitat types were represented, including several types of
Mediterranean scrub, agricultural lands, dehesas (savannah-like formations that
combine pastures with intermittent cereal cultivation in park-like oak woodlands;
Blondel and Aronson 1999) and forests containing various tree species (e.g. Pinus sp.
and Quercus pyrenaica).
Variable selection
From each study we derived the following parameters: respective geographical variables
(latitude and longitude, in degrees; and altitude, in metres) either from the study itself
or, if they were not provided in the study, from Google Earth (http://earth.google.com);
the source of food materials analysed (scats or stomach contents); and the simple size,
study duration, season, habitat, and FO of each food group (see Appendices 1.1. and
1.2.). We categorized dietary items into the following main groups: lagomorphs (mainly
European wild rabbits; see Results), small mammals (rodents and insectivores), birds,
reptiles, invertebrates, fruits/seeds, and carrion/garbage (mainly large mammals and
leftover food of anthropogenic origin). Four seasons were considered: spring (March–
May), summer (June–August), autumn (September–November) and Winter (December–
February). The habitat type at each location was categorized as Mediterranean scrub,
forest or agricultural–dehesa (agricultural land and dehesas), according to the
descriptions given in each study. We calculated Herrera’s trophic diversity index (D;
Herrera 1976) from the FO data as an index of the trophic diversity for each diet. The
index is computed according to the formula 퐷 = −∑ logpi, where p is the
frequency of occurrence of the various prey categories (i). This index is recommended
for presence–absence food data, because other diversity indices such as the Shannon
index cannot be calculated from this type of data (Herrera 1976).
To test for bias caused by the study duration, sample size or source of analysed food
material (scats or stomach contents; Putman 1984), we followed the approach of earlier
authors (Lozano et al. 2006; Zhou et al. 2011) and used multivariate analysis of
covariance with the study duration and simple size as covariates, food material as a
fixed factor and the FO of each of the seven food groups as response variables.
35
To avoid temporal pseudo-replication, we considered only those studies in which annual
information on the Iberian fox diet was provided: 30 studies and localities, including a
total of 9459 samples (stomachs and scats; see Appendix 1.1. and 1.2.). Therefore,
analyses of the relationship of the consumption of various food groups to geographical
variables and habitat type were performed using the anual data base. The testing of
seasonal variation was based only on those studies in which seasonal data were
reported: 18 studies and 20 localities, including a total of 5027 samples (stomachs and
scats; see Appendices 1.1. and 1.2.).
The relationships between geographical variables (latitude, longitude and altitude) and
the FO of each food group were tested using simple regression analyses. In view of the
potential importance of wild rabbits in the diet of red foxes, we used a simple regression
analysis to investigate the relationships between the lagomorph FO (mainly wild
rabbits; see Results) and the FO of other food groups. To evaluate whether trophic
specialization occurred in Iberian red foxes, we tested the relationships between diet
diversity (Herrera D index) and the FO of each of the four main food groups
(lagomorphs, small mammals, invertebrates and fruits/ seeds) using data from annual
studies. We applied general linear models (GLMs) using a normal distribution for errors
of the response variable (Herrera D index) and an identity link function. One-way
analysis of variance was used to test the effect of habitat type on the FO of each food
group. We assessed seasonal variations in the diet by performing separate one-way
analyses of variance with the FO of each food group as a dependent variable. We
conducted Tukey’s post-hoc tests to assess differences between pairs of habitat types
and seasons.
Prior to statistical analyses, the FO for each food group and the Herrera D index values
(dependent variables) were arc sine and log transformed, respectively, to achieve
normality (Zar 1984), which was assessed visually from normal probability plots. All
statistical analyses were performed using Statistica 6.0 software (StatSoft 2001).
Results We found no significant effect of study duration (F7,26 = 0.86, P = 0.55), sample size
(F7,26 = 0.73, P = 0.64), source of analysed food material (scats or stomach contents;
F7,26 = 0.43, P = 0.11) or the interaction between sample size and food material (F7,26 =
1.04, P = 0.42) on the FO of food groups in the diet. Thus, for further analyses we
36
pooled data from studies with differing durations, sample sizes and sources of analysed
food material.
Overal diet
Iberian red foxes consume a wide range of food items. Invertebrates were the most
frequent food group in their diet (mean FO±SD, 40.1±25.5%), followed by fruits/ seeds
(38.9±22.0%), small mammals (34±20.9%), lagomorphs (20.6±22.0%), carrion/garbage
(15.3±14.2%), birds (13.4±15.3%) and reptiles (1.8±2.8%).
Coleoptera and Orthoptera species were the most common among the invertebrates, and
both wild and cultivated fruits were included among the fruits/sedes consumed. The
most common small mammal prey was Apodemus sylvaticus, followed by Microtus
spp., Crocidura spp. and Eliomys quercinus. Wild rabbit was the dominant species
among the lagomorphs, while hares Lepus spp. Were rare in the red fox diet (only
identified in 6 of the 27 studies that recorded lagomorphs; FO = 1.2±0.43%). For this
reason, we will use indistinctly ‘rabbits’ and ‘lagomorphs’ from now on in the text. The
large mammals reported as fox food items included Cervus elaphus, Dama dama, Sus
scrofa, Bos taurus, Ovis aries and Capra hircus, and were presumably consumed as
carrion. Among birds in the fox diet, the most common species consumed were
Columba spp., Alectoris rufa, Galerida spp. and Anas spp. Several reptile species were
consumed, including Psammodromus spp., Malpolon monspessulanus and Elaphe
scalaris.
Geographical patterns (latitude, longitude and altitude)
We found a negative and statistically significant relationship between latitude and the
FO of lagomorphs (R2 = 0.19, F1,35 = 8.47, P = 0.006; Figure 1.2a.) and invertebrates
(R2 = 0.11, F1,35 = 4.37, P = 0.04; Figure 1.2b.), and a positive and significant
relationship between latitude and the FO of small mammals (R2 = 0.16, F1,35 = 6.78, P =
0.01; Figure 1.2c.) and fruits/sedes (R2 = 0.12, F1,35 = 5.04, P = 0.03; Figure 1.2d.).
Therefore, at lower latitudes, lagomorphs and invertebrates were more frequently eaten,
while at higher latitudes small mammals and fruits/seeds were more commonly
consumed.
Only the FO of invertebrates and fruits/seeds were significantly related to longitude.
The consumption of invertebrates increased towards the east (R2 = 0.12, F1,35 = 4.95, P =
0.03), whereas that of fruits/seeds increased towards the west (R2 = 0.16, F1,35 = 6.99, P
= 0.01).
37
Figure 1.2. Relationships between latitude and the frequency of occurrence (FO; arc sine
transformed) of (a) lagomorphs (b) invertebrates (c) small mammals and (d) fruits/seeds in the
diet of the red fox. Each point represents one study site (see Figure 1.1.).
Altitude was significantly and negatively associated with the FO of lagomorphs (R2 =
0.29, F1,30 = 12.67, P = 0.001; Figure 3a), and positively associated with that of small
mammals (R2 = 0.27, F1,30 = 11.31, P = 0.002, Figure 1.3b.). Thus, the consumption of
lagomorphs decreased with altitude, and that of small mammals increased.
Is the red fox specialized on rabbits in the Iberian Peninsula?
The consumption of wild rabbits (represented by lagomorphs) was significantly and
negatively related to the consumption of both small mammals (R2 = 0.15, F1,35 = 6.23,
P = 0.02) and fruits/seeds (R2 = 0.17, F1,35 = 8.41; P = 0.006). The GLM results suggest
that diet diversity was not significantly associated with latitude (F1,25 = 0.33, P > 0.5),
altitude (F1,25 = 0.552, P > 0.4) or the FO of the four main food groups (lagomorphs:
F1,25 = 0.126, P > 0.7; small mammals: F1,25 = 0.004, P > 0.9; invertebrates: F1,25 = 0.253,
P > 0.6; and fruits/seeds: F1,25 = 0.196, P > 0.6).
0.0
0.2
0.4
0.6
0.8
1.0
1.2
1.4
1.6
Lago
mor
ph R2 = 0.19
0.0
0.2
0.4
0.6
0.8
1.0
1.2
1.4
1.6
Smal
l mam
mal
s
R2 = 0.16
36 37 38 39 40 41 42 43 44
Latitude
0.0
0.2
0.4
0.6
0.8
1.0
1.2
1.4
1.6
Inve
rtebr
ates
R2 = 0.11
36 37 38 39 40 41 42 43 44
Latitude
0.0
0.2
0.4
0.6
0.8
1.0
1.2
1.4
1.6
Frui
t/See
d
R2 = 0.12
a c
db
0.0
0.2
0.4
0.6
0.8
1.0
1.2
1.4
1.6
Lago
mor
ph R2 = 0.19
0.0
0.2
0.4
0.6
0.8
1.0
1.2
1.4
1.6
Smal
l mam
mal
s
R2 = 0.16
36 37 38 39 40 41 42 43 44
Latitude
0.0
0.2
0.4
0.6
0.8
1.0
1.2
1.4
1.6
Inve
rtebr
ates
R2 = 0.11
36 37 38 39 40 41 42 43 44
Latitude
0.0
0.2
0.4
0.6
0.8
1.0
1.2
1.4
1.6
Frui
t/See
d
R2 = 0.12
a c
db
38
Figure 1.3. Relationships between altitude (in metres) and the frequency of occurrence (FO; arc sine transformed) of (a) lagomorphs and (b) small mammals in the diet of the red fox. Each point represents one study site (see Figure 1.1.).
Habitat type and seasonality
We found a significant relationship between habitat type and the FO of lagomorphs
(F2,21 = 8.10, P = 0.002) and small mammals (F2,20 = 4.05, P = 0.03) in red fox diet. The
FO of lagomorphs was higher in Mediterranean scrub than in forest (Figure 1.4a.), but
the opposite was observed for small mammals (Figure 1.4b.).
A significant seasonal relationship in the red fox diet was found for reptiles (F3,53 =
3.34, P = 0.02), invertebrates (F3,53 = 9.45, P < 0.0001) and fruits/seeds (F3,53 = 11.49, P
< 0.0001). The FO of reptiles increased from winter to summer (Figure 1.5a.);
invertebrates were mostly consumed in summer, and their occurrence in the diet was
lowest in winter (Figure 1.5b.); and fruits/seeds were consumed most in autumn and
0.0
0.2
0.4
0.6
0.8
1.0
1.2
1.4
Lago
mrp
h
R2 = 0.29a
0 200 400 600 800 1000 1200 1400 1600
Altitude
0.0
0.2
0.4
0.6
0.8
1.0
1.2
1.4
Sm
all m
amm
als
R2 = 0.27b
0.0
0.2
0.4
0.6
0.8
1.0
1.2
1.4
Lago
mrp
h
R2 = 0.29a
0.0
0.2
0.4
0.6
0.8
1.0
1.2
1.4
Lago
mrp
h
R2 = 0.29a
0 200 400 600 800 1000 1200 1400 1600
Altitude
0.0
0.2
0.4
0.6
0.8
1.0
1.2
1.4
Sm
all m
amm
als
R2 = 0.27b
0 200 400 600 800 1000 1200 1400 1600
Altitude
0.0
0.2
0.4
0.6
0.8
1.0
1.2
1.4
Sm
all m
amm
als
R2 = 0.27b
39
least in spring (Figure 1.5c.). Marginally significant differences were found for
lagomorphs (F3,53 = 2.40, P = 0.07), which were consumed most in summer (Figure
1.5d.).
Figure 1.4. Frequency of occurrence (FO; arc sine transformed; means±SE) of (a) lagomorphs and (b) small mammals in the diet of the red fox as a function of habitat type. Means marked with the same letter are not significantly different from one another (P < 0.05; Tukey’s post-hoc test). M. scrub, Mediterranean scrub; Agri., agricultural lands.
M. Scrub Forest Agri./Dehesa0.00.10.20.30.40.50.60.70.80.91.0
Sm
all m
amm
als
0.0
0.1
0.2
0.3
0.4
0.5
0.6
0.7
0.8
0.9
1.0La
gom
orph
sa
b
A
A, B
B
(N=12) (N=9) (N=3)
A A, B
B
M. Scrub Forest Agri./Dehesa0.00.10.20.30.40.50.60.70.80.91.0
Sm
all m
amm
als
0.0
0.1
0.2
0.3
0.4
0.5
0.6
0.7
0.8
0.9
1.0La
gom
orph
sa
b
A
A, B
B
(N=12) (N=9) (N=3)
A A, B
B
40
Figure 1.5. Frequency of occurrence (FO; arc sine transformed; means±SE) of (a) reptiles (b) invertebrates (c) fruits/seeds and (d) lagomorphs in the diet of the red fox, as a function of season (marginally non-significant for lagomorphs, P = 0.07). Means marked with the same letter are not significantly different from one another (P < 0.05; Tukey’s post-hoc test).
Discussion Biogeographical variations in the diet of the red fox in Iberia
Generalist predators feed on different food resources according to their abundance and
availability (Futuyma and Moreno 1988). This study confirms that the red fox is a
generalist predator; its trophic patterns can be explained by geographical variables,
habitat type and seasonality. These factors determine directly the abundance and
availability of its main foods [e.g. wild rabbits are more abundant at southern latitudes
(Villafuerte et al. 1998) and in Mediterranean scrubland habitats (Calvete et al. 2004);
small mammals are more abundant at northern latitudes (Soriguer et al. 2003) and in
forest habitats (Torre et al. 2002)]. Latitude influences the feeding patterns of many
medium-sized carnivores (Clavero et al. 2003; Hounsome and Delahay 2005; Lozano et
al. 2006; Zhou et al. 2011). Some researchers relate dietary patterns in the abundance
and diversity of prey species with the latitudinal gradient described in Eurasia, which
Winter Spring Summer Autumn0.00.10.20.30.40.50.60.70.80.91.0
Lago
mor
phs
Winter Spring Summer Autumn0.00.10.20.30.40.50.60.70.80.91.0
Frui
ts/S
eeds
0.00
0.05
0.10
0.15
0.20
0.25R
eptil
es
0.00.10.20.30.40.50.60.70.80.91.01.11.2
Inve
rtebr
ates
a b
c d
A
A, B
B
A
A, BB, C
C
A
B
A, CC
A
A, B
B
(N=11) (N=15) (N=18) (N=13) (N=11) (N=15) (N=18) (N=13)
A, B
A, B
Winter Spring Summer Autumn0.00.10.20.30.40.50.60.70.80.91.0
Lago
mor
phs
Winter Spring Summer Autumn0.00.10.20.30.40.50.60.70.80.91.0
Frui
ts/S
eeds
0.00
0.05
0.10
0.15
0.20
0.25R
eptil
es
0.00.10.20.30.40.50.60.70.80.91.01.11.2
Inve
rtebr
ates
a b
c d
A
A, B
B
A
A, BB, C
C
A
B
A, CC
A
A, B
B
(N=11) (N=15) (N=18) (N=13) (N=11) (N=15) (N=18) (N=13)
A, B
A, B
41
increases towards the south (Pianka 1966; Blondel and Aronson 1999). Our results are
consistent with these findings as we observed a latitudinal gradient in the consumption
of lagomorphs, invertebrates, small mammals and fruits/seeds by red foxes.
The increase in the consumption of lagomorphs, mainly wild rabbits, towards southern
Iberia is a consequence of the greater abundance of this prey at these latitudes
(Villafuerte et al. 1998). The same pattern in rabbit intake has been shown for other
medium-sized Iberian carnivores including the wildcat (Lozano et al. 2006), the badger
(Virgós et al. 2005; Barea-Azcón et al. 2010) and the polecat (Santos et al. 2009). This
feeding pattern could explain the negative latitudinal gradient found in the body size of
Iberian red foxes, which contradicts Bergmann’s Rule (Yom-Tov et al. 2007). The high
occurrence of invertebrates in the red fox diet in southern regionsmay be explained by
the greater availability of this food type at low latitudes (Chapman 1998; Blondel and
Aronson 1999) and is in agreement with studies of the diet of other medium-sized
Iberian generalist carnivores including the genet (Virgós et al. 1999).
The positive relationship between latitude and small mammal consumption by Iberian
red foxes corresponds to a south–north gradient in the abundance and species richness
of this prey group (Blanco 1998; Soriguer et al. 2003). The decrease in rabbit abundance
in northern regions of the Iberian Peninsula also promotes the switch to small mammals
as the main prey in these areas. This pattern was also observed by Zhou et al. (2011) in
Holarctic marten species at a larger biogeographical scale.
The consumption of fruits/seeds by the red fox is greater in northern regions than in
southern regions. However, this pattern is opposite to that described for other Eurasian
generalist carnivores, which decrease their consumption of plant matter and increase
carnivory with increasing latitude (Virgós et al. 1999; Goszczynski et al. 2000; Vulla et
al. 2009; Zhou et al. 2011). In some of these studies, this pattern is explained by a
reduction in primary production with increasing latitude, but the narrow latitudinal
range covered in the present study leads us to believe that the higher consumption of
fruits/seeds is likely to be due to the greater availability of this resource in the north of
the Iberian Peninsula.
The FO of invertebrates in the fox diet increases from east to west, while that of
fruits/seeds increases from west to east. Rosalino and Santos-Reis (2009) were not able
to explain a similar longitudinal gradient found in fruit/seed consumption by medium-
42
sized carnivores in Iberia because of the absence of data on the availability of plant
species producing fruits and seeds. Invertebrates are an alternative food source for some
omnivorous species, especially larger carnivorous mammals, where larger prey items
are not available (Capinera 2010). However, as there is currently no information on the
availability of invertebrates over a longitudinal gradient in Iberia, we have no data to
enable us to interpret our results.
The decrease in consumption of lagomorphs by foxes with increasing altitude could be
because of the reduced presence and abundance of rabbits above 1000m (Blanco 1998;
Palomo et al. 2007), but the consumption of small mammals by foxes increased in high
altitude areas. This is in contrast with previous findings that the species richness and
abundance of small mammals decreases at higher altitudes (Torre 2004). However, the
altitudinal range considered in this study (only three localities were higher than 1400m;
see Appendix S1) did not include altitudes that may limit the presence of most small
mammals consumed by the red fox (Palomo et al. 2007), which prevents us from
confirming this trend in small mammal consumption. Thus, the increased intake of
small mammals seems to be a functional response to the reduced availability of
lagomorphs at higher altitudes, as Hartová-Nentvichová et al. (2010) found for red
foxes in the mountains of the Czech Republic.
Is the red fox specialized on rabbits in the Iberian Peninsula?
A negative relationship between a given food group and dietary diversity is usually
interpreted as indicating trophic specialization (Futuyma and Moreno 1988; Fedriani et
al. 1998; Lozano et al. 2006). A negative relationship at a regional scale between
lagomorph consumption and dietary diversity has been described for red foxes (Delibes-
Mateos et al. 2008) and for other small and medium-sized Mediterranean carnivores
(Sarmento 1996; Lozano et al. 2006; Santos et al. 2009). However, we did not find any
significant relationship between dietary diversity and the consumption of lagomorphs or
other prey, or geographical variables, perhaps because of the high trophic flexibility of
the fox in the Iberian Peninsula. These results suggest that, at the scale of the peninsula,
only small mammals and fruits/seeds are eaten by foxes as alternatives to lagomorphs.
This confirms the opportunistic and generalist feeding behaviour of the red fox, as has
consistently been reported for different geographical areas and at various scales (e.g.
Kjellander and Nordstrom 2003, Dell’Arte et al. 2007).
43
Habitat type and seasonality
We observed a high intake of lagomorphs by red foxes in the Mediterranean scrubland,
where wild rabbits reach higher densities (Fedriani 1996; Palomares 2001; Calvete et al.
2004). In contrast, Fedriani (1996) found no difference in consumption of wild rabbits
by red foxes in adjacent áreas of scrubland and dehesa habitat in Doñana (southwest
Iberian Peninsula), despite higher rabbit density in the scrubland patches. This is
probably a consequence of the larger scale considered in our review, where habitats
were clearly differentiated between studies. The preference for forests shown by the
small mammal species most frequently consumed by foxes (e.g. Apodemus sylvaticus;
Torre et al. 2002), together with the low abundance of rabbits in this type of habitat,
explains why foxes include in their diet a greater proportion of small mammals in
forests than in others habitats.
Several researchers have reported marked seasonality in the diet of the red fox
(Dell’Arte et al. 2007; Hartová-Nentvichová et al. 2010). Mediterranean ecosystems
have marked climatic seasonality, with hot dry summers and cold wet winters (Blondel
& Aronson 1999); thus, some trophic resources for carnivores are only seasonally
available (Virgós 2002). We also observed a marked seasonality in the diet of the red
fox, which is a result of the seasonal availability of some food groups at the Iberian
scale. Populations of Orthoptera and Coleoptera, the invertebrates most consumed in
summer, increase dramatically during this season (Aranda et al. 1995; Loureiro et al.
2009). The availability of cultivated and wild fruits is greatest in summer and autumn
(Loureiro et al. 2009), when they are most consumed by foxes. The annual abundance
of wild rabbits in the Iberian Peninsula peaks in the spring–summer period (Soriguer
1981; Beltrán 1991). At this time the greater availability of juvenile rabbits and the
susceptibility of the rabbit population to myxomatosis (Calvete et al. 2002) may make
this prey more vulnerable to predation and consumption as carrion by foxes, so that
rabbits may provide a valuable energy source for foxes during the highly critical
breeding period. This explains the observed seasonal increase in the FO of lagomorphs
from spring to summer (Figure 1.5d.). However, in areas where rabbits are very
abundant, their availability is high throughout the year (Angulo and Villafuerte 2003),
which could explain the lack of statistically significant differences between seasons in
the FO of lagomorphs in the red fox diet.
44
Conclusions
Biogeographical variation in the feeding habits of Iberian red foxes are associated with
geographical variables, hábitat type and season, which affect the availability of
alternative potential foods (Figure 1.6.). Our results confirm that the feeding habits of
the red fox, a generalist predator, vary widely both spatially and temporally, even within
a relatively small biogeographical area such as the Iberian Peninsula. Therefore, we
demonstrate that the flexibility of this generalist predator really reflects the
biogeographical patterns of distribution and abundance of its main food sources.
Understanding these patterns in the feeding ecology of the red fox, the most abundant
carnivore in the Iberian Peninsula, will facilitate the understanding of the geographical
variations in its abundance and behaviour, and improve the management and
conservation of this species.
Figure 1.6. Conceptual model illustrating the biogeographical patterns found in the
consumption of the main food groups by the Iberian red fox, in relation to geographical
variables (LAG, lagomorphs; SM, small mammals; F/S, fruits/seeds; INV, invertebrates). The
white arrows represent latitudinal (LATITUDE) and longitudinal (LONG) gradients, and the
grey arrow shows the altitudinal gradient (ALTITUDE).
45
Acknowledgements We are especially grateful to Drs P. C. Alves and C. Gortázar for providing unpublished
data to be included in this review. We thank also Drs. Jennings and Hackländer, and
two anonymous referees whose comments greatly improved the manuscript. M.
Delibes-Mateos currently holds a Juan de la Cierva research contract awarded by the
Ministerio de Ciencia e Innovación and the European Social Fund. C. Ferreira was
supported by a PhD grant (Ref. SFRH/BD/22084/2005) funded by the Fundação para a
Ciência e Tecnologia of the Ministério da Ciência, Tecnologia e Ensino Superior,
Portuguese government. Financial support for the study was provided by the Spanish
MICINN Project CGL2009-10741 from Spanish Plan Nacional de I+D and FEDER
funds.
46
CAPÍTULO 2: Factors affecting the feeding habits of black-billed magpies Pica pica during the breeding season in Mediterranean Iberia
Este capítulo ha sido enviado a una revista SCI:
Díaz-Ruiz F, Zarca JC, Delibes-Mateos M., Ferreras (enviado) Factors affecting the feeding habits of black-billed magpies Pica pica during the breeding season in Mediterranean Iberia.
47
Abstract Feeding habits of the black-billed magpie are of conservation and management interest
for researchers, conservationists and hunters since magpies are considered as predators
of eggs and chicks of both songbirds and gamebirds. The aim of this study was to
characterize the feeding habits of magpies during the breeding season of birds (i.e.
magpies and sympatric birds) in agricultural environments of central Spain, and to
assess the occurrence and incidence of birds and eggs in the magpie’s diet. Diet was
determined by the analysis of gizzards contents from 118 magpies. We tested the effect
of locality, age and sex on diet composition and diet diversity through multivariate
analysis of variance (MANOVA) and general lineal models (GLM). Magpies presented
a generalist diet, which included a wide range of foods. Arthropods and cereal seeds
were the most frequent food groups (frequency of occurrence, FO >60 %). Eggs and
birds were consumed only occasionally (FO < 6% and 17% respectively; percentage of
volume, VOL, < 4%), and more frequently during magpie incubation stage. We did not
find overall significant differences in diet related with age and sex. Significant effects
were only found for the interaction between sex and age and between them and locality.
Our findings suggest that magpies do not seem to pose an important threat for the
conservation of birds in Mediterranean agricultural environments, under the conditions
found during this study. Nevertheless, more complex studies in different scenarios (i.e.
different population sizes of magpies and prey) and at longer temporal scales are
necessary to clarify this controversial issue.
Key words: bird conservation, egg predation, feeding habits, generalist diet, predator
control
48
Introduction Feeding habits is an important and widely studied aspect of animal ecology and a
fundamental component for understanding the biology and ecology of species. Some
species are perceived as harmful for human interests, frequently because of their feeding
habits. For instance, some predators can consume species of human interest such as
game species or livestock (Woodroffe et al. 2005). From this point of view, the
information provided by studies on predator feeding habits may be relevant to guide
appropriate policy and management decisions (López-Bao et al. 2013) that facilitate
human-wildlife coexistence.
Feeding habits of the black-billed magpie (Pica pica, hereafter the magpie) give rise to
controversial interpretations between researchers, conservationists and hunters. In
Europe, magpies are considered as a harmful bird species by some conservationists and
hunters because of their predation on eggs and chicks of songbirds and gamebirds
(Birkhead 1991; Herranz 2000). As a consequence, control of magpie populations is
widespread in Europe (Hadjisterkotis 2003), particularly in southern regions (Chiron
and Julliard 2013; Díaz-Ruiz and Ferreras 2013). In Spain, magpie control is mostly
performed by hunters and game managers, who consider magpies as high efficient
predators of nests of red-legged partridges (Alectoris rufa) (Delibes-Mateos et al. 2013;
Díaz-Ruiz and Ferreras 2013), a small game species of socioeconomic relevance (Díaz-
Fernandez et al. 2012).
Magpies feeding habits have been object of several studies focusing on different issues,
e.g. seasonal diet composition, food selection, diet of nestlings or differences between
feeding patterns of rural and urban magpies (Birkhead 1991; Soler and Soler 1991;
Martínez et al. 1992; Ponz et al. 1999; Kryštofková et al. 2011). These studies describe
magpies as generalist predators that feed on a broad spectrum of food types. In general,
eggs form only a small proportion of magpie diet (Birkhead 1991; Martínez et al. 1992),
although some studies have shown that magpies are one of the main predators of
artificial and natural nests (Groom 1993; Herranz 2000; Miller and Hobbs 2000; Roos
and Pärt 2004). Nevertheless, the impact of magpies on bird populations remains still
unclear, due to contrasting results (Gooch et al. 1991; Stoate and Szczur 2001; Thomson
et al. 1998; Chiron and Julliard 2007; Newson et al. 2010), particularly in the Iberian
Peninsula, where the number of studies on this issue is low. In addition, other basic
49
aspects of the feeding habits of magpies, such as how these are affected by intrinsic
factors (e.g. age or sex) remain largely unknown.
Differences in feeding behaviour related to age and sex have been shown for several
vertebrate species, e.g. reptiles (Liu et al. 2011), mammals (Kidawa and Kowalczyk
2011) and birds (Le Vaillant et al. 2013). In bird species, foraging behaviour may differ
between males and females, in order to avoid intraspecific competition for food
resources (Le Vaillant et al. 2013). Moreover, individuals improve with age their
knowledge of the environment and their ability to prospect for food, which means that
older individuals can expand the range of available dietary items, or focus on more
profitable foods, increasing their foraging efficiency (Pärt 2001; Gomes et al. 2009).
Biometrical differences occur between sexes and age classes in magpies; males are
larger than females and adults are larger than yearlings (Birkhead 1991; Martínez 2011).
Furthermore, during the breeding period males and females take on different roles, e.g.
only females incubate (Buitron 1988). In addition, magpies can remember the type of
food they hoarded, in which location, and when this hoarding took place (Zinkivskay et
al. 2009), and this ability may be more accentuated in more experienced adult birds than
in yearlings. Therefore, these biological and behavioural differences linked to age and
sex may be a source of variation in the magpie’s diet as observed in the case of other
birds (Le Vaillant et al. 2013; Pärt 2001; Gomes et al. 2009). On the one hand, larger
individuals may capture larger prey, such as birds, and more experienced individuals
may have learned to exploit resources not used by less experienced individuals, such as
nests. Although these aspects may be very relevant for magpies’ management, they have
not been tested or described so far for this species.
In the present study or main goal was to characterize the diet of magpies during their
breeding season in agricultural rural areas of central Iberia. Our specific aims were to
examine: (1) the occurrence and importance of birds and eggs in the diet of magpies and
(2) whether age, sex and area may be sources of variation in the feeding habits of
magpies.
Material and Methods Study Area
Magpie feeding habits were studied in two hunting estates located in central Spain
(Area 1: 960 ha, 39º 4.5´ N, 3º 54´ W; Area 2: 547 ha, 39º 33´ N, 3º 12´ W), during
50
spring 2006. Both study areas were within the Mediterranean bioclimatic region (Rivas-
Martínez et al. 2004), and were similar in habitat composition: an agricultural
dominated landscape with some interspersed patches of natural vegetation (mainly
Mediterranean bushes and some trees in riparian areas and hedgerows). Main crops
were cereals (~50 and 70% of total surface) and, to a lesser extent, vineyards and olive
groves. Hunting was an important activity in both estates, and the main game species
were Iberian hare (Lepus granatensis), European wild rabbit (Oryctolagus cuniculus)
and red-legged partridge. Partridge density was low in both estates (less than 0.36
partridges/ha, authors, unpublished data), within the range of other agricultural regions
of the Iberian Peninsula (Borralho et al. 1996; Duarte and Vargas 2001). Both hunting
estates harbor an important community of small breeding birds, including species of
families such as Alaudidae or Fringillidae (Martí and Del Moral 2003). Magpie density
in both study areas (Area 1: 0.23 magpies/ha, Area 2: 0.39 magpies/ha, before breeding
season; see Díaz-Ruiz et al. 2010) was above average values reported in other areas of
Europe (Birkhead 1991).
Sample collection
Magpies were captured during an experimental evaluation of cage-traps as live capture
methods for magpie population management (see for more details Díaz-Ruiz et al.
2010). Magpies were captured during their breeding season of 2006 (Birkhead 1991;
Soler et al., 1999; Ponz and Gil-Delgado 2004): during May in Area 1 and during late
May-early June in Area 2. Birds were euthanized using standard procedures and
following current guidelines of animal welfare (Close et al. 1997). Age was determined
from the shape and appearance of the first outermost primaries; this method allows to
differentiate between first-year (hereafter young) and older magpies (hereafter adult)
(Erpino 1968; Birkhead 1991). Sex was determined for each individual by the
assessment of gonadal development during laboratory necropsies. Gizzard contents
were extracted and placed in 70% alcohol in labeled plastic tubes for subsequent
analyses.
Gizzard contents analysis
Magpie diet was determined through the analysis of gizzard contents, a frequent
methodology used in diet study of several bird species (Jiguet 2002; Kopij 2005; Bur et
al. 2008). Gizzard contents were analysed in the laboratory following the methodology
51
described in corvid diet studies (Soler et al. 1990; Soler and Soler 1991; Herranz 2000).
Food items were identified to the lowest possible taxonomic level using published
literature (Day 1966; Barrientos 1988; Devesa 1991; Teerink 1991; Chinery 1997), as
well as a dedicated reference collection of seeds, invertebrates, bird eggs and mammal
hairs. The thickness of eggshells was measured with a digital calliper (precision 0.01
mm) to assign the eggs at least to the family level (Herranz 2000). All identified items
were pooled in nine food classes: arthropod, gastropod, cereal seed, fruit, other vegetal,
bird, egg, reptile and mammal, and two non-food items: gastrolith and plastic (Table
2.1. and Appendix 2.1.). We estimated the minimum number of individuals per food
class present in each gizzard by: the presence of whole individuals or diagnostic hard
structures (e.g. thorax, elytrum, chelicerae or heads) for invertebrates; cereal grain husk
and fruit seeds; for vertebrates we assumed a minimum number of one since usually
only feathers, hair or small fragments of eggshell appeared.
We calculated three dietary indices frequently used in diet studies (Soler et al. 1993;
Herranz 2000; Hadjisterkotis 2003; Kryštofková et al. 2011): the frequency of
occurrence (FO) expressed as the percentage of gizzards in which a food item was
found, the relative frequency of occurrence (RF) expressed as the percentage of times a
food item occurs in relation to the total times all food items occur, and the percentage of
volume (VOL) estimated as the percentage of total volume corresponding to a certain
food item upon the total content of each gizzard.
Data analysis
We used VOL of each food class in the statistical analyses because this index considers
the amount of each food class in each magpie gizzard. The individual gizzard was
considered as the sampling unit in the statistical analyses. In order to test the effect of
study area, age (adult or young) and sex on diet composition and diversity we conducted
two statistical approaches.
First, we pooled all food classes in four main categories to avoid groups with very low
FO (< 5 %; e.g. fruits, reptiles and mammals). The four categories were: invertebrates
(arthropods and gastropods), cereal seeds, vegetal (encompassing fruits and other
vegetal material, see below) and vertebrates (eggs, birds, reptiles and mammals). We
used multivariate analysis of variance (MANOVA) with the VOL of each main food
category as response variables and the study area, age and sex and all interactions
52
between them as fixed factors. Using these main categories, we calculated diet diversity
of each gizzard using the Shannon diversity index(퐻 = ∑ 푝푖 lg푝푖). Differences in
퐻′ were tested using General Linear Models (GLM), which included the same factors as
in MANOVA.
Second, we assessed the factors explaining the consumption of the principal food
classes (FO ≥ 5%) present in both study areas (arthropod, cereal seed, other vegetal,
gastropod, bird and egg). For this, we performed independent GLMs with the VOL of
each food class as dependent variable and study area, age, sex and all interactions as
fixed factors.
A negative relationship between a given food and dietary diversity is usually interpreted
as indicative of trophic specialization (Futuyma and Moreno 1988). We tested whether
magpies specialize on any food class through Pearson´s correlation analysis between the
principal food classes (FO ≥ 5%) and H’.
Prior to statistical analyses, the VOL for each food class and H’ values (dependent
variables) were log (x+1) transformed to achieve normality (Zar 1984), which was
assessed visually from normal probability plots of residuals. All statistical analyses
were performed using Statistica 10.0 software (Statsoft INC 2011) and the significance
level was set at α = 0.05.
Results A total of 118 gizzards were collected and analyzed in the laboratory, achieving a
similar sample size for each study area (61 from Area 1, 57 from Area 2), age (51 adult,
67 young), and sex (48 females, 70 males). Overall, we identified 1016 food items in
the gizzard contents belonging to 26 taxonomic groups (Table 2.11 and Appendix 2.1.).
Diet composition
Magpies consumed a wide range of food items among which arthropods and cereal
seeds were the most frequent classes (total FO of 94.07% and 66.95% respectively),
followed by other vegetal (FO of 33.90%) and birds (FO of 16.95%). Other food classes
(gastropods, mainly small snails, bird eggs, fruits, mammals and reptiles) were present
in lower FO (< 10%, Table 2.1. and Appendix 2.1.). Coleoptera and formicidae species
represented 90% of the items consumed among the artrhropoda (Appendix 2.1.). We
were able to identify 84% of the seeds found in the gizzards, and most of them
53
corresponded to Hordeum sp. (64%), Avena sp. (27%) and Triticum sp. (9%) (Appendix
2.1.). The “other vegetal” class was composed mainly by grass stalk and leaves of
unidentified herbaceous plants, likely from cereal crops. We only could differentiate
bird remains to the taxonomic order level by the microscopic structure of feathers (Day
1966). Most bird remains belonged to passeriformes (n = 15), and only one of them
corresponded to galliformes (Appendix A). Bird egg remains always appeared highly
fragmented, making very difficult the identification of the species that had produced
them. Nevertheless, according to the thickness of eggshells, four (< 0.09 mm) were
compatible with eggs produced by small birds (likely passeriformes), one (0.14 mm)
with those of doves and one with those of partridges (0.23 mm, Herranz 2000). The rest
of vertebrate prey items were remains of two Apodemus sylvaticus, hairs of one Felis
sp., and one undetermined mammal and reptile species, respectively (Appendix 2.1.).
Table 2.1. Magpie diet composition in central Spain. For each food class, we present the
number of gizzards containing remains (Gizzards), the frequency of occurrence (FO) and the
average % volume (VOL). Data is independently presented in terms of overall magpie diet
(Total) and for each study area (A1 and A2). More detailed data on diet composition are shown
in the Appendix 2.1.
Gizzards FO VOL
Food class Total
(n = 118) A1
(n = 61) A2
(n = 57) Total A1 A2 Total A1 A2
Arthropoda 111 56 55 94.07 91.80 96.49 41.14 29.16 53.96
Gastropoda 11 10 1 9.32 16.39 1.75 3.07 5.89 0.05
Cereal seeds 79 43 36 66.95 70.49 63.16 36.10 36.43 35.75
Fruits 5 5 0 4.24 8.20 0.00 1.55 3.00 0.00
Other vegetal 40 27 13 33.90 44.26 22.81 10.75 16.20 4.93
Eggs 6 5 1 5.08 8.20 1.75 2.63 3.61 1.58
Birds 20 17 3 16.95 27.87 5.26 3.87 5.90 1.70
Mammals 4 4 0 3.39 6.56 0.00 0.07 0.13 0.00
Reptiles 1 1 0 0.85 1.64 0.00 0.21 0.41 0.00
Influence of locality, age and sex on diet composition and diversity
Our first approximation showed that overall diet varied significantly between study
areas and that there was a statistically significant effect of the sex-area interaction, and a
marginal statistical effect of the interaction sex-age on diet variation (Table 2.2.). Only
54
VOL of seeds did not differ between localities (Tukey post-hoc, Appendix 2.2.). Males
fed similarly in both areas but females from Area 1 fed more on vegetal and less on
invertebrates than females from Area 2 (Tukey post-hoc; Appendix 2.3.).
Table 2.2. Results of MANOVA using the four main food categories as response variables:
invertebrates (arthropod and gastropod), cereal seeds, vegetal (encompassing fruit and other
vegetal material, see below) and vertebrates (egg, bird, reptile and mammal) and three fixed
factors (Study Area, Age and Sex) and all possible interactions. Statistically significant
variables are highlighted in bold and marginally significant ones in italic.
Variables Value F4, 107 P-value Study Area 0.75 9.15 < 0.001 Sex 0.94 1.71 0.154 Age 0.98 0.68 0.609 Study Area*Age*Sex 0.97 0.82 0.513 Study Area*Sex 0.88 3.48 0.010 Study Area*Age 0.98 0.63 0.645 Sex*Age 0.92 2.38 0.056
Significant differences in the consumption of principal food classes were mainly related
to the study areas (Table 2.3.). Magpies consumed more arthropods, less other vegetal,
less gasthropods and less birds in Area 2 than in Area 1 (Figure 2.1.). The only
significant difference due to sex was a larger consumption of other vegetal by females
(mean ± se: 15.11±2.93) than males (7.89±2.39). The interactions between sex and area
significantly affected the consumption of arthropods (Figure 2). The effect of the
interaction sex-age on the consumption of other vegetal group VOL was statistically
significant (Table 2.3.; Figure 2.3.).The consumption of bird eggs was not significantly
affected by any of the factors considered.
Magpie diet was significantly more diverse in Area 1 than in Area 2 (Table 2.3.; Figure
2.4.), while sex, age and interactions did not represent significant differences in diet
diversity (Table 2.3.). H’ was significantly and positive correlated with the VOL of
cereal seeds and other vegetal material (Pearson´s correlation: 0.36 and 0.39
respectively; p < 0.05). VOL of arthropods was significantly and negatively correlated
with VOL of cereal seeds, eggs, birds and vegetal groups (Pearson´s correlation: -0.40, -
0.33, -0.24 and -0.20 respectively; p < 0.05).
55
Table 2.3. Results of the General Linear Models (GLMs) performed to assess the effect of different factors on the consumption of the principal food classes (FO ≥ 5%) by magpies and on diet diversity (H´). Degrees of freedom were 1,110 in all F tests. Statistically significant variables are highlighted in bold.
Diet Diversity (H´) Arthropoda Cereal Seeds Vegetal Gastropoda Birds Eggs
Variables F p F p F p F p F p F p F p
Study Area 16.04 0.014
25.35 <0.001
0.34 0.560
12.67 0.001
5.87 0.017
6.26 0.014
0.93 0.336 Sex 0.17 0.677
1.40 0.239
1.83 0.179
7.11 0.009
0.05 0.830
0.91 0.342
0.03 0.860
Age 1.17 0.280
0.48 0.491
2.19 0.142
0.37 0.543
0.05 0.826
0.08 0.773
0.03 0.867 Study Area*Sex*Age 0.01 0.888
0.26 0.614
0.06 0.812
1.33 0.252
1.80 0.183
1.08 0.301
0.39 0.535
Study Area*Sex 0.02 0.874
7.98 0.006
1.51 0.222
2.50 0.116
0.28 0.598
0.07 0.793
0.77 0.382 Study Area*Age 1.98 0.874
0.85 0.358
0.05 0.820
0.05 0.823
0.01 0.927
0.60 0.438
1.49 0.224
Sex*Age 2.13 0.147 0.88 0.351 0.88 0.351 4.90 0.029 2.74 0.101 2.34 0.129 2.81 0.097
56
Figure 2.1. Percentage of volume (VOL; mean±SE) of the principal food classes (FO > 5%)
consumed by magpies in both study areas. *: Statistically significant differences; NS: non-
significant differences.
Figure 2.2. Variation in the percentage of volume of arthropods (VOL) consumed by magpies
(mean±SE) in function of the study area and sex. *: Statistically significant differences between
pair of means (Tukey’s post-hoc test); NS: non-significant differences (Tukey’s post-hoc test).
57
Figure 2.3. Variation in the percentage of volume (VOL) of vegetal food consumed by
magpies (mean±SE) in function of age and sex. *: Statistically significant differences between
pair of means (Tukey’s post-hoc test); NS: non-significant differences (Tukey’s post-hoc test).
Figure 2.4. Differences in magpie diet diversity (H´; means±SE) between study areas.
58
Discussion Our findings show that, during the breeding season, magpies fed on different food
types, with varying importance between localities, and that the most frequently
consumed food classes were cereal seeds and arthropods. This is in agreement with
previous studies conducted in Spain, which indicated that, although both food classes
are consumed throughout the year, the consumption of invertebrates increases during
the breeding season, when their availability is higher (Soler and Soler 1991; Martínez et
al. 1992; Herranz 2000).
Magpie predation on eggs and birds
Eggs were detected in a low proportion and volume in magpie gizzards (< 6%), in
accordance with most previous studies (Birkhead 1991). A higher occurrence of eggs in
magpie diet has been recorded in a previous study conducted in central Spain (FO = 13-
20 %; Herranz 2000); a large proportion of these were attributed to red-legged
partridges (77-80 %). In contrast, only one of the egg remains found in our study (17%)
coincided with the partridge egg thickness. This suggests that partridge eggs do not
represent an important food for magpies during the breeding season in the study areas.
However, several studies conducted in the Iberian Peninsula have shown that magpies
are one of the main predators of dummy partridge nests (Herranz 2000; Blanco-Aguiar
et al. 2001; Ferreras et al. 2010). From this perspective, we cannot discard that magpie
nest predation could represent a risk for partridge breeding success in a scenario of high
magpie abundances and low partridge densities, where even a small number of partridge
eggs predated by each magpie could represent a large impact on the breeding success of
the partridge population. In addition, partridge nest predation by magpies may be
underestimated in diet studies, which hardly detect remains of predated eggs, i.e.,
eggshells (Chiron and Julliard 2007). This is probably because magpie behaviour of egg
predation and ingestion varies with egg size. Thus, while smaller eggs are entirely
swallowed, including the eggshell, larger ones are broken and only the egg content and
small eggshell pieces are swallowed (Suvorov et al. 2012), decreasing the likelihood of
eggshells ingestion.
We found a relatively high consumption of passerines (12.7 % FO) compared with data
reported in other studies performed during the breeding season (FO < 8 %; Birkhead
1991; Herranz 2000; Kryštofková et al. 2011). It has been suggested that magpie
59
predation on breeding birds may be related to high bird densities (Birkhead 1991).
However, Fernández-Juricic et al. (2004) found that magpie predation on birds was
opportunistic and was mainly observed during the breeding season, regardless of bird
abundance. Magpies might increase their predatory pressure on birds when
invertebrates, the principal animal component of their diet, are less available.
Sources of magpie diet variation and consumption of other food groups
The consumption of the other main food groups, except cereal seeds and eggs, varied
between localities. This pattern was potentially related to food availability, as suggested
by the similar consumption of cereal seeds between areas, which had similar cereal crop
surfaces. Nevertheless, we must be cautious with this interpretation for two reasons.
First, we did not have data about the availability of the other food groups, and second
magpies can select food items independently to their availability; e.g. some invertebrate
groups (Martínez et al. 1992; Kryštofková et al. 2011). Alternatively, differences in the
consumption of arthropods, birds and eggs between areas may be explained by the
different breeding stages when samples (i.e. gizzards) were collected: during the
incubation stage in Area 1 and during the stage of nestling feeding in Area 2. In this
sense, Suvorov et al. (2012) showed that magpies predated dummy nests more
frequently at the incubation stage than during the stage of nestling feeding because
during this stage magpies select invertebrates to feed nestlings (Martínez et al. 1992).
This may also explain the lower diet diversity found in Area 2. During our study an
important proportion of young magpies were also reproductive (all captured young
females showed brood patch, indicating they were breeders), and therefore this may
explain that young magpies presented a similar feeding behavior to adults.
Globally, we did not find differences in diet composition associated with age and sex,
and only the interaction between the locality and these intrinsic factors significantly
affected magpie diet. During the breeding season males regularly feed females (Buitron
1988), so it would be expected that the diet was similar between sexes. However, we
observed that adult females included in their diet significantly more vegetal food than
adult males. Breeding females spend most of the time in the nest during incubation and
hatching (Buitron 1988), where vegetal food, which they can easily consume, is
probably more available, supplementing food provided by males. Also, female magpies
consumed more arthropods than males in Area 2. During the nestling feeding stage
60
males increase the supply of food to the female and chicks (Buitron 1988), being
invertebrates the main food brought to chicks (Martínez et al. 1992; Ponz et al. 1999).
In this sense, the male probably reduces the consumption of invertebrates in order to
provide most of their catch to the nest.
Magpie diet diversity
Our results indicate that magpies do not specialize in any food during our study since
diet diversity was not related negatively to the occurrence of any of the main food
classes (Futuyma & Moreno 1988). In contrast, diet diversity was positively related to
the amount of cereal seeds and other vegetal in the diet. This suggests that magpies need
to supplement their diet including many different animal food types, although it is
predominantly vegetarian. Invertebrates are the principal contribution of protein in a
large number of birds (Capinera 2010), including magpies in agricultural landscapes
within central Spain. Arthropods consumption was negatively associated with the
consumption of other animal sources of proteins, such as birds or eggs, suggesting that
these may be a secondary and occasional source of protein for magpies during the
breeding season (Birkhead 1991).
Conclusions
Overall we found no evidence that magpies pose a threat to the conservation of birds
since magpies include in their diet eggs and birds in a low proportion, regardless of the
age and sex of magpies. However, the possible sources of bias associated with our study
methodology, such as the quantification of these bird remains and eggs, as well as the
fact that even a low rate of predation may affect a prey when the predator is abundant,
make us to be cautious with this conclusion. Thus, more complex and experimental
studies at larger time-spatial scales are necessary, including localities with different
densities of magpies and potential bird prey. Diet data should be complemented with the
monitoring of the abundances of potential bird prey species and magpies, prey breeding
success and predation rate of magpies on nests, chicks and adults birds.
Acknowledgements We are very grateful to land owners and game managers who allowed us to work in
their hunting estates. We thank people who assisted us during the fieldwork, especially
S. Luna and L.E. Minguez. We acknowledge Dr. J.T. García and Dr. E. Pérez-Ramírez
for necropsy and sexing of magpies. This study was funded by Consejería de Medio
61
Ambiente of Junta de Comunidades de Castilla-La Mancha (Project PREG-05-23). M.
Delibes-Mateos is currently supported by a JAE-DOC contract funded by CSIC and the
European Social Fund.
Ethical standards This work was performed in compliance with current Spanish legislation, and follows
the European Union’s recommendations regarding animal welfare. All procedures were
carried out with all legal permits required by the concerned administrations.
62
CAPÍTULO 3: An evaluation of cage-traps and the Collarum device to capture red foxes (Vulpes vulpes). Can the performance of cage-traps be improved by baits and scent attractants?
Este capítulo se encuentra en preparación para ser enviado a una revista SCI:
Díaz-Ruiz F, Delibes-Mateos M., Ferreras P (en preparación) An evaluation of cage-traps and the Collarum device to capture red foxes (Vulpes vulpes). Can the performance of cage-traps be improved by baits and scent attractants?
63
Abstract Carnivore predation on prey of human interest, such as game species or livestock, leads
frequently to the lethal control of predators. This constitutes a serious conservation
problem in many places across the world, since non-target species of conservation
concern are frequently removed. In Spain, cage-trapping is one of the most widespread
methods used by hunters to control red foxes (Vulpes vulpes), although its low
efficiency and selectivity have been frequently reported. From this perspective, these
control methods need urgently to be improved, and its performance compared to that of
new alternative devices, such as the Collarum restraint device. The aim of this study
were to test whether the use of different baits and scent attractants may improve the
selectivity and efficiency of cage-traps, to compare the performance of different cage-
traps designs with that of the Collarum restraint device, and to analyse the injuries
caused by both methods to captured animals. Fieldwork was conducted in three study
sites in central Spain during 2003 and 2006/07. We tested the effect of two types of
baits (dead or alive), four scent attractants, and their combinations on the efficiency and
selectivity of three cage-trap types commonly used to control foxes in Spain. During
2006/07, we also compared the Collarum restraint device with cage-traps in terms of
efficiency and selectivity. Injuries caused to animals by both capture methods were also
described. Cage-traps captured a total of six foxes and 40 individuals of 13 non-target
species, including protected carnivores and raptors, with an overall effort of 2068 trap-
nights. The use of live baits and fox urine increased the efficiency of cage-traps
independently of the cage-trap type. In addition, the capture rate of non-target animals
was lower with cage-traps with chamber for bait adjacent to the capture chamber and
with traps of one capture chamber. It was also slightly lower using valerian scent as
attractant. The Collarum restraint device was more selective (50-100%) than cage-traps
(12-29%) and more efficient than cage-traps without attractant, but as efficient as cage-
traps with attractants. Animals captured with both types of traps showed no indicator of
poor welfare. Our results suggest that live baits and scent attractants may improve the
efficiency and selectivity of cage-traps for capturing red foxes. Even so, non-target
species, including some protected ones, can be still captured, and selectivity levels are
still very low (0-21%) and therefore the use of this method is not recommended for
managing foxes in Spain. The Collarum restraint device may be an acceptable selective
alternative to traditional methods in areas with similar carnivore composition than that
64
existing in our study sites. Further studies are necessary to test the selectivity in other
areas with different composition of carnivore communities. Although our results show
that the selectivity of trapping methods can be improved, the decision of releasing
captured non-target animals depends ultimately on the trapper. For this reason, it is of
key importance that fox management is carried out by skilled technical personnel and
always supervised by wildlife competent authorities.
Keywords: red fox, cage-traps, Collarum restraint device, capture efficiency, selectivity, predator control, game management.
65
Introduction Lethal control of predators is widespread all over the world (Treves and Karanth 2003;
Woodroffe et al. 2005), because humans usually see these species as competitors for
shared, limited resources, such as game species (e.g. Valkama et al. 2005) or livestock
(e.g. Treves et al. 2004; Sangay and Vernes 2008). Intensive predator removal has
caused the local extinction of several species of conservation concern, and massive
contractions of the geographic ranges of many others (e.g. Whitfield et al. 2003).
Methods of predator control may result in the death of protected species. On the one
hand, some legal methods are not selective, and therefore non-target protected species
are captured (e.g. Duarte and Vargas 2001; Way et al. 2002). On the other hand, come
managers employ illegal, unselective methods, such as poisoning (e.g. Whitfield et al.
2003; Márquez et al. 2012), based on their belief that legally permitted methods are not
efficient to reduce predator numbers (Delibes-Mateos et al. 2013).
The removal of predator species of conservation concern causes frequent clashes
between conservationists and hunters and game managers (Virgós et al. 2010). In
biodiversity conflict management, success occurs when the outcome is acceptable to
both sides and when neither party is asserting its interests to the detriment of others
(Redpath et al. 2013). Under this perspective, banning totally predator control would not
be the best way to minimise conflicts between hunters and conservationists in relation to
predator management. In this regard, finding efficient and selective control methods to
legally reduce the numbers of some generalist/opportunistic predators could help to
reduce these tensions between hunters and conservationists.
In Spain, hunting is a very important socioeconomic activity and one of the most
important leisure rural activities; thus, >77 % of the territory is covered by hunting
estates (Rios-Saldaña 2010; Arroyo et al. 2012). Hunters and game managers employ
several different management tools, including predator control, to boost game species
numbers (see Angulo 2003; Arroyo et al. 2012). The use of predator control is
widespread in some Spanish regions (Ríos-Saldaña 2010; Díaz-Ruiz and Ferreras 2013).
For example, in central Spain most small-game estates (~ 90%) use some type of
predator control (Delibes-Mateos et al. 2013). The main predators legally controlled in
Spain are red foxes (Vulpes vulpes), feral cats (Felis catus) and feral dogs (Canis lupus
familiaris), among carnivores, and magpies (Pica pica), among birds. Nevertheless, the
detrimental effect of illegal predator control on some protected species of conservation
66
concern, including raptors and carnivores, has been frequently reported (e.g. Villafuerte
et al. 1998; Márquez et al. 2013).
Spanish hunters argue frequently that the current legal predator control methods are
inefficient, and therefore they request more effective methods to cull predators, and
especially red foxes (Delibes-Mateos et al. 2013). For example, cage-traps, which are
one of the most frequently employed methods to legally control foxes are usually
considered as inefficient by Spanish hunters (Delibes-Mateos et al. 2013). In fact, the
efficiency of cage-traps to capture foxes in Spain is extremely low; capture rate ranges
between 1.2 and 5 foxes per 1000 trap-nights, and levels of selectivity are far from
acceptable (Herranz 2000; Duarte and Vargas 2001; Muñoz-Igualada et al. 2008). Given
that this is neither acceptable for conservationists (selectivity) nor for hunters
(efficiency), it is urgent to explore possibilities of improving both the efficiency and
selectivity of cage-traps in Spain. For example, some scent attractants could be used to
achieve this goal, since not all the species respond equally to different scent attractants
(Monterroso et al. 2011). In addition, Iberian predators show different feeding
strategies; some species feed exclusively on live prey (e.g. the European wildcat (Felis
silvestris); Lozano et al. 2006), while others can also scavenge (e.g. red fox; Díaz-Ruiz
et al. 2013). This suggests that the probability of capturing different species could
change in function of the type of bait (alive or dead) used. To our knowledge, only
Herranz (2000) previously tested for differential attraction effects using both dead and
alive baits in Spain, but this author did not evaluate any scent attractant.
Methods alternative to cage-traps have been used to capture other canids with success in
terms of efficiency, selectivity and injuries to both target and non-target. For example,
the Collarum restraint device (hereafter Collarum), a powered neck snare designed to
the live capture of canids (see Shivik et al. 2000), has shown up to 87% efficiency for
coyotes (Canis latrans; Shivik et al. 2005). In Spain, the Collarum has been tested for
capturing foxes only in two studies developed in northern and southern Spain
respectively (Muñoz-Igualada et al. 2008; Andalucía 2010). These studies consider the
Collarum as highly selective and its efficiency as higher than that of traditional cage-
traps (Muñoz-Igualada et al. 2008), but still far from the efficiency obtained for coyotes
(Shivik et al. 2005).
67
In this paper, our goals were: 1) to evaluate the efficiency and selectivity of different
types of cage-traps traditionally used for the capture of red foxes in Spain; 2) to test
whether the use of different baits and scent attractants improve the selectivity and
efficiency of different cage-traps types; 3) to compare the performance of cage-traps
and the Collarum restraint device in terms of efficiency and selectivity; and 4) to
describe the injures caused to foxes and non-target species by both capture methods.
Material and Methods Study areas
Fieldwork was performed in 3 sites of central Spain (Ciudad Real province), one private
and two public estates, during 2003 and 2006/2007 (Table 3.1.). The climate was typical
Mediterranean characterised by wet, mild winters and warm, dry summers with a
marked drought period (Rivas-Martínez et al. 2004). The landscape was similar between
study sites i.e. Mediterranean scrubland (mainly Cistus spp. in combination with holm
oak (Quercus ilex) forests), mixed with cereal croplands, riparian habitats, ‘dehesas’
(pastureland with savannah-like open tree layer, mainly dominated by Mediterranean
evergreen oaks) and pine (Pinus spp.) plantations (Table 3.1.).
Study sites selection was based on three criteria: 1) a high habitat heterogeneity that
favoured the presence of a diverse wildlife community, including both prey and
predators, 2) a medium-high red fox abundance, which allowed us to test trap efficiency
for capturing foxes, and 3) a high diversity of other potentially capturable predators,
including protected ones, which allowed us to asses trap selectivity.
The three study sites were situated in the distribution area of several Iberian terrestrial
carnivores such as European wildcat, stone marten (Martes foina), small-spotted genet
(Genetta genetta) and Eurasian badger (Meles meles); the Egyptian mongoose
(Herpestes ichneumon) was also present in Site 1 (Palomo et al. 2007). Our study sites
also held raptors, such as common buzzards (Buteo buteo), goshhawks and
sparrowhawks (Accipiter sp.), Bonelli's eagles (Aquila fasciata), Spanish Imperial
eagles (Aquila adalberti), Golden eagles (Aquila chrysaetos) or Eagle owls (Bubo bubo)
(Martí and Del Moral 2003).
68
Table3.1. Description of study sites. The geographical location, the year and season when trapping was performed are shown.
Study site Location Year (Season) Area (ha) Main habitat types Main land uses
Site 1 38˚27´40´´N 3˚34´5´´ W
2003 (September-November)
3700 Pine plantations (Pinus pinaster), Mediterranean scrub (Cistus sp.), holm oak forest (Quercus ilex), and cereal crops
Managed publicly for forestry production and big game
Site 2 38˚ 58 ́2´ ́N 4˚ 8´47´´ W
2006 (July-December)
1000
“Dehesa” (a typical Mediterranean formation of sparse oaks and underlying cereal crops), holm oak forest with Mediterranean scrub, and riparian vegetation
Managed privately for livestock, cereal agriculture, and big game
Site 3 39˚ 0 ́2´ ́N 4˚ 23´55´´ W
2006/2007 (November-March) 1500 “Mixed” forests of pine (Pinus sp.) and holm
oak with Mediterranean scrub. Managed publicly for forestry, and small and big game
69
The presence of these species and foxes was previously confirmed by the technical staff
of the public estates (i.e. Sites 1 and 3; Junta de Comunidades de Castilla-La Mancha,
unpublished data), by colleagues from our Institute (Site 2, P. Acevedo, unpublished
data), and during the revision of the traps in this study. Since no direct measure of the
abundance of potentially capturable species was available, we performed nocturnal
spotlight-counts chiefly to estimate fox relative abundance (kilometric abundance index,
KAI) at the beginning of the study and during the trapping season (Ruette et al. 2003).
KAIs estimated were apparently higher in site 2 (0.26 foxes km-1, 42.4 km surveyed)
than in site 1 (0.016 foxes km-1, 60 km surveyed), and in site 3 (0.02 foxes km-1, 66.4
km surveyed). The European wildcat (Felis silvestris) was only observed in Site 1,
(0.016 wildcats km-1), and feral cats in Site 3 (0.03 km-1).
Efficiency and selectivity definitions of control methods
We used the parameters described previously by the International Organization for
Standardization (1999) for testing restraining traps for mammals. The number of foxes
captured per 1000 trap-nights was used to assess trapping system efficiency. We
evaluated two parameters related to the selectivity: direct selectivity, or the percentage
of foxes captured related to the total number of animals captured (including red foxes),
and the non-target capture rate, or number of non-target captures per 1000 trap-nights
(inversely related to selectivity).
Trap types evaluated
We used three types of cage-traps used in Spain for capturing foxes. These types had
one or two capture entrances that employed a guillotine-type door and a tread trigger
system, differing in design details. CT01 type had one entrance and one capture
chamber; used exclusively with dead baits placed in the capture chamber, CT02 type
had two entrances, one capture chamber and a lateral bait chamber and CT03 type had
two entrances, two capture chamber and a central bait chamber (see Appendix 3.1.).
Some of these types included different commercially available models that slightly
differed in their characteristics, such as measures or mesh size, as described in
Appendix 3.1.
The Collarum neck restraint device is a specific trap to selectively capture canids, such
as coyotes, foxes, dogs and dingoes (Canis lupus dingo) (Shivik et al. 2000, 2005). It
70
uses a baited pull-tab that triggers a pair of coil-spring powered throw-arms that propels
a cable loop over the head onto the neck of a fox (Muñoz-Igualada et al. 2008). We
tested the commercially available red fox version (Wildlife Control Supplies, East
Granby, Connecticut, USA). The Collarum traps were tested in Sites 2 and 3.
Baits and scent attractants
We tested two types of bait (dead or alive) for possible effects on the efficiency and
selectivity of cage-traps. Chicken carcasses and lamb meat were used as dead baits.
Common quails (Coturnix coturnix), red legged partridges (Alectoris rufa), and
helmeted guinea fowl (Numida meleagris) were used as live baits. Dead baits were
placed inside the traps secured with wire to avoid that animals took them away, and
they were weekly replaced. Live baits were placed in an independent chamber that was
adjacent to, or inside the trap, depending on the trap model (see Appendix 3.1.).
We also tested the effect of scent attractants on cage-trap efficiency and selectivity. We
tested four types of scent attractants previously used to attract red foxes (Saunders and
Harris 2000; Monterroso et al. 2011): red fox urine (hereafter FU), valerian-extract
solution (hereafter VAL), containing valeric acid found in urine and anal-sac secretions
of fox (Albone and Fox 1971; Jorgenson et al. 1978), fatty acids scent (hereafter FAS),
a mixture of seven volatile fatty acids found in fermented eggs (Roughton 1982), and
Collarum canine bait (Wildlife Control Supplies, East Granby, Connecticut, USA;
hereafter COLL), a commercial canids-specific attractant. Scent attractants were
impregnated on a piece of chalk tied to an iron stick with elastic bands, driven to the
ground inside the cage-trap. The chalk was moistened with the attractant (1-5 cc) with
the help of a syringe and was replenished every 3-4 days.
Dead and live baits were tested in all study sites, but only FU and VAL scent attractants
were used in all study sites. FAS was tested in Sites 2 and 3, and COLL only in Site 3.
Moreover, traps without any scent attractant were used as control in all the localities.
We followed a block design in each study site, with the treatment randomly assigned to
each trap within a block, regardless of the trap type. Three treatments were
simultaneously tested in Site 1: control, FU and VAL. Four treatments were tested in
Site 2, control and three scents (FU, VAL and FAS) being simultaneously deployed
after an initial period with the control treatment in all the traps. Five treatments were
simultaneously tested in Site 3: control, FU, VAL, FAS and COLL. The minimum
71
distance between neighbouring traps was 100 m. Traps were placed near shrubs or other
resources that increase the probability of animal presence (e.g. ponds, water courses,
edges of dense vegetation, etc.).
Handling of animals and injuries
All captured animals were examined in situ by a wildlife veterinarian for possible trap-
related injuries. For veterinarian inspection, both foxes and non-target carnivores
captured were immobilized with a combination of Ketamine hydrochloride (50 mg/ml,
Imalgene ® 50, Merial) and Xylazine hydrochloride (20 mg/ml Rompun®, Bayer); this
was injected intramuscularly in the animal's hindquarters, using recommended doses for
small and medium size carnivores (15 mg Ketamine + 1-1.5 mg Xylacine per Kg; Seal
and Kreeger 1987). To do so, animals were transferred from the cage-trap to a squeeze
cage that allows their physical immobilization, and prevent damage to both them and
the veterinary (Ferreras et al. 1994). Non-target carnivores were marked with a
subcutaneous transponder (ID-100, Trovan®), which allowed their identification in case
of recapture. The drug effect was reversed using Yohimbine (0.15 mg per Kg; Seal and
Kreeger 1987). Once fully recovered from anesthesia and after the veterinary checked
that no serious injuries compromised their survival, animals were released in the capture
site (Harris et al. 2006).
A correct evaluation of injuries caused by trapping methods to target species requires
the examination through a post-mortem necropsy of at less 20 captured animals
(European Union-Canada-Russian Federation 1998; United States of America-European
Community 1998; International Organization for Standardization 1999). In our study,
the number of captured foxes was <20, and only three foxes were euthanized; the others
were kept in captivity for subsequent behavioural experiments. Therefore, we only were
able to show a descriptive list of the injuries observed by the veterinary in situ. Injuries
were recorded according to the four categories established in the international scale of
traumas: mild trauma, moderate trauma, moderate-severe trauma and severe trauma
(International Organization for Standardization 1999). The method chosen for
euthanizing foxes was the intravenous injection of T61 ® (Intervet), which is the
method recommended for euthanizing dogs and cats due to its high speed, efficiency,
ease of use and safety (Close et al. 1996; 1997; Gómez-Villamandos 2000). All
72
procedures were performed following approval by the competent authority (Castilla-La
Mancha Regional Government).
Statistical Analyses
Cage-traps, baits and attractants
Generalized Linear Mixed Models (GLMMs) were employed to analyze the effect of
cage-trap type, and different baits and scent attractants on the efficiency and selectivity
of the cage-traps. The individual trap with each combination of baits and attractants was
utilized as the sample unit. In this analysis, the number of foxes captured in 1000 traps-
nights was used as a measure of efficiency (Muñoz-Igualada et al. 2008). Since direct
selectivity could not be calculated in many individual traps that produced no capture at
all, non-target capture rate was used as a measure inversely related to selectivity
(Muñoz-Igualada et al. 2008). Due to violations of normality and variance homogeneity
of standardized residuals, dependent variables (i.e. efficiency and non-target capture
rate) were square-root (x+1) transformed (Muñoz-Igualada et al. 2008). FAS and COLL
scent attractants were excluded from these analyses because they were not employed in
all study sites.
Fixed factors included as explanatory variables in these models were: cage-trap type
(CT01, CT02 and CT03), bait type (dead or alive), scent attractant (control, FU and
VAL), and the interaction between bait and scent attractants. Study site was included as
a fixed factor because number of levels was not enough to be considered as a random
variable (Zuur et al. 2007). Since a given trap received several different treatments (bait
x attractant), trap location (a categorical variable identifying each trap position in the
fieldi.e. trap id) was included as a random variable in the models.
Collarum vs. cage-traps
Differences in the efficiency and non-target capture rate between cage-traps and
Collarum were tested in Sites 2 and 3. In order to simplify the analysis we grouped
cage-traps in those with and without scent attractant. Generalized Linear Mixed Models
(GLMMs) were developed to test for differences between cage-traps and Collarum in
terms of efficiency and non-target capture rate. The type of trapping device
(CT_control, CT_attractant or Collarum) and the study site (Site 2 and 3) were included
in these models as fixed factors. Trap location was included as a random effect.
73
All statistical analyses were performed using the lme4 package of the R statistical
software (Bates and Maechler 2010; R Core Development Team 2013). The models
were obtained with the function dredge of MuMin package (Barton 2012) and compared
through the AICc criterion (Burnham and Anderson 2002). The coefficients of predictor
variables were calculated through model-averaging (Burnham and Anderson 2002). We
present the coefficient of variables resulting from the model-averaging for all models
with a total cumulative weight of at least 90% (Arnold 2010).
Results Overall captures
A total effort of 3359 trap-nights produced the capture of 9 red foxes and 41 non-target
animals of 13 species. Cage-traps captured a total of 6 foxes and 40 non-target animals,
including carnivores, raptors, corvids and other game species, with an overall values of
efficiency and selectivity of 2.9 foxes/1000 trap-nights and 13 % respectively (Table
3.2.). Collarum traps captured 3 foxes and one non-target animal, with overall values of
efficiency and selectivity of 2.3 foxes/1000 trap-nights and 75 % respectively (Table
3.2.).
Baits and scent attractants
Cage-traps captured foxes with both types of baits, and using all attractants except with
COLL and FAS (Figure 3.1.). Model-averaging for efficiency included eight models
with a total cumulative weight of 90% (Table 3.3.). The explicative variables in order of
relative importance were study site (0.96), scent attractant (0.78), bait (0.66), the
interaction bait*scent attractant (0.47) and trap type (0.10). Capture rate of red foxes
was higher in Site 2 (mean±SE: 18.51±13.11 foxes/1000 trap-nights) than in the two
other sites (Site 1: 0.83±0.83, and Site 3 without captures; Table 3.4.). Only the
interaction live bait*FU increased the efficiency of cage-traps to capture red foxes
(Table 3.4.; Figure 3.1.).
Non-target species were captured using cage-traps with both types of bait and all the
attractants except COLL (Table 3.3.). Model-averaging for non-target captures included
eight models with a total cumulative weight of 91% (Table 3.3.). The explicative
variables in order of relative importance were trap type (1), scent attractant (0.84), bait
(0.52), study site (0.30) and the interaction bait*scent attractant (0.26). Cage-trap types
74
CT01 and CT02 had a lower non-target capture rate than CT03 type, and VAL attractant
produced a slightly lower capture rate of non-target species than FU and control (Table
3.4.; Figure 3.1.).
75
Table 3.2. Number of animals captured in the three study sites using cage-traps and Collarum devices, and the selectivity and efficiency of both methods.
The total sampling effort, estimated as the number of trap-nights, is shown. Efficiency is the number of foxes captured in 1000 trap-nights. Selectivity is the
percentage of foxes captured related to the total number of animals captured (included red foxes). Non-target CR is capture rate refers to the number of non-
target animals captured per 1000 trap-nights. Vv: red fox, Fs: European wildcat, Gg: European genet, Mf: stone marten, Hi: Egyptian mongoose, Mm:
European badger, Ag: goshawk, Fc: feral cat, Clf: dog, and Others: Black-billed magpie (n= 1), azure magpie (n= 1), wild boar (n= 2), red-legged partridge
(n= 19) and European wild rabbit (n= 1).
Trap type Study Site Year Trap-Nights Vv
Non Target captures
Efficiency Non-target CR Selectivity Fs Gg Mf Hi Mm Ag Fc Clf Others Total
Cage-traps
Site 1 2003 601 1 0 2 0 2 1 0 0 0 2 7 1.6 11.6 12.5
Site 2 2006
810 5 1 1 0 0 0 1 0 3 15 21 6.17 25.9 19.2
Site 3 657 0 2 2 1 0 0 0 1 0 6 12 0 18.3 0
Overall 2068 6 3 5 1 2 1 1 1 3 23 40 2.9 19.3 13
Collarum Site 2
2006 362 1 0 0 0 0 0 0 0 0 1 1 2.8 2.8 50
Site 3 929 2 0 0 0 0 0 0 0 0 0 0 2.2 0 100
Overall 1291 3 0 0 0 0 0 0 0 0 1 1 2.3 0.77 75
TOTAL 3359 9 3 5 1 2 1 1 1 3 24 41
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Table 3.3. Best models explaining the efficiency of cage-traps 1) for capturing foxes, and 2)
for capturing non-target animals using different baits and scent attractants. AIC values of the set
of GLMMs included a total cumulative weight of at least 0.90.
Table 3.4. Model-average coefficients and standard errors (SE) of the variables included in the
models explaining the efficiency of cage-traps to capture red fox and non-target animals. The
intercept includes Site 2, live bait, control attractant and CT03 cage-trap type.
Red fox Non-target
Variable Parameter SE Parameter SE Intercept 2.19*** 0.58 7.45*** 0.98 Site 1 -1.22* 0.61 -0.53 1.13 Site 3 -1.58** 0.51 -0.36 0.85 Alive bait 0.15 0.61 0.47 0.89 FU 0.16 0.60 -0.91 0.83 VAL 0.18 0.65 -1.63# 0.90 Alive bait*FU 1.80* 0.91 -0.60 1.51 Alive bait*VAL 0.03 0.99 -0.11 1.64 CT01 0.15 0.78 -4.26*** 1.14 CT02 -0.12 0.53 -5.58*** 0.85 *p<0.05; **p<0.01; ***p<0.001
# p= 0.07
Model d.f.
Log-Like AICc Delta AICc weight
1) Fox site+bait+attractant+bait*attractant 10 -160.6 344.1 0.00 0.33
site+attractant 7 -165.0 345.5 1.45 0.16
site 5 -167.7 346.2 2.12 0.11
site+bait+attractant 8 -164.4 346.6 2.54 0.09
site+bait 6 -166.9 346.8 2.75 0.08
site+bait+attractant+trap type+bait*attractant 12 -159.7 347.7 3.64 0.05
bait+attractant+trap type+bait*attractant 8 -165.2 348.3 4.24 0.04
site+bait+attractant+trap type 9 -164.1 348.6 4.56 0.03
2) Non-target
trap type+attractant 7 -203.3 422.1 0.00 0.24
bait+trap type+attractant+bait*attractant 10 -199.8 422.6 0.54 0.18
bait+trap type+attractant 8 -202.6 423.0 0.94 0.15
site+trap type+attractant 9 -201.6 423.5 1.48 0.11
site+bait+trap type+attractant+bait*attractant 12 -198.0 424.4 2.35 0.07
trap type 5 -206.9 424.6 2.49 0.07
site+bait+trap type+attractant 10 -200.8 424.6 2.56 0.07
site+trap type 7 -205.0 425.4 3.35 0.04
77
Figure 3.1. Average capture rate (±SE) (indv./1000 traps-nights) observed of both foxes and
non-target animals captured with cage-traps using each type of bait (dead and alive) and scent
attractants (Control: without attractant; FU: fox urine; VAL: valerian-extract; FAS: fatty acids
scent; COLL: Collarum canine bait). Data of captures using FAS and COLL as attractants are
shown, although these were not included in GLMMs analyses.
Cage-traps vs. Collarum
Capture rate of red foxes using both types of devices was higher in Site 2 (14.51±10.01
foxes/1000 trap-nights) than in Site 3 (0.91±0.61 foxes/1000 trap-nights) (Table 3.5.).
The efficiency for capturing foxes differed between cage-traps and Collarum (Table
3.5.; Figure 3.2.); the average red fox capture rate was 3.24±1.97 foxes/1000 trap-nights
using the Collarum, 0.87±0.86 foxes/1000 trap-nights using cage-traps without scent
attractants and 6.34±4.86 using cage-traps with scent attractants (Table 3.5.; Figure
3.2.). Additionally, the capture rate of non-target species was significantly lower with
Collarum (0.45±0.44 captures/1000 trap-nights) than that obtained with cage-traps
either with scent attractants (11.39±5.66 captures/1000 trap-nights) or without scent
attractants (23.46±11.25 captures/1000 trap-nights) (Table 3.5.; Figure 3.2.).
78
Table 3.5. Model standardized coefficients and standard errors (SE) for cage-traps with and
without scent attractants (CT_Attractant and CT_Control, respectively) vs. Collarum analysis of
efficiency of red fox captures and non-target captures. Intercept includes Site 2 and CT_Control.
Red fox Non-target
Variable Parameter SE Parameter SE
Intercept 1.94** 0.41 3.66** 0.73
Site 3 -1.40* 0.41 -1.12 0.76
CT_Attractant 0.72 0.43 -0.88 0.66
Collarum 0.74 0.50 -1.62* 0.83 *p<0.05; **p<0.01
Figure 3.2. Means and SE of the observed capture rates of foxes and non-target animals
(indv./1000 trap-nights) using cage-traps with and without scent attractants (CT_Attractant and
CT_Control, respectively) and the Collarum restraint device in sites 2 and 3.
Injuries
None of the tested traps caused any serious injury or the death (i.e. severe trauma in ISO
scale) of the red foxes captured. However, 83% and 100% of foxes captured with cage-
traps and Collarum, respectively, showed injuries, corresponding to nine mild or
moderate traumas (International Organization for Standardization 1999; Table 3.6.).
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Most of the non-target animals captured with the cage-traps showed no injuries (76 %;
n= 31). In the rest of the individuals, seven categories of injuries were detected, and on
most occasions these referred to mild or moderate traumas, with the exception of two
cases of severe traumas (Table 3.6.). Only one azure magpie died as a consequence of
severe trauma (i.e. neck fracture caused by the trap door; Table 3.6.). The Collarum
device captured only one non-target species, a wild boar, causing it “major cutaneous
laceration” and death (Table 3.6.).
80
Table 3.6. Observed injuries in animals captured using cage-traps and Collarum devices. Data were obtained through veterinarian “in situ” inspections.
Injuries recorded in the list of the International Organization for Standardization (1999) are shown: *Severe trauma category; the other injuries showed are
included into Mild or Moderate trauma categories. Vv: red fox, Fs: European wildcat, Gg: European genet, Mf: stone marten, Hi: Egyptian mongoose, Mm:
European badger, Ag: goshawk, Fc: feral cat, Clf: domestic dog, Pp: black-billed magpie, Cc: azure magpie, Ss: wild boar, Ar: red legged partridge and Oc:
European wild rabbit.
Cage traps
Collarum
Vv
(n=6) Fs
(n=3) Gg
(n=5) Mf
(n=1) Hi
(n=2) Mm
(n=1) Fc
(n=1) Cld
(n=3) Pp
(n=1) Ag
(n=1) Ss
(n=1) Cc
(n=1) Ar
(n=19) Oc
(n=1) Vv
(n=3) Ss
(n=1) Injury
Claw damaged 0 1 1 0 0 1 1 0 0 0 0 0 0 0 0 0 Oedematous swelling or hemorrhage 2 1 1 0 0 0 1 0 0 0 0 0 0 0 3 0
Minor cutaneous laceration 1 2 2 0 1 0 0 0 0 0 0 0 0 0 0 0
Minor subcutaneous soft tissue maceration or erosion (contusion)
1 1 2 0 0 0 0 0 0 0 0 0 0 0 0 0
Major cutaneous laceration, except on foot pads or tongue
0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1
Chipped or fracture of a permanent tooth without exposing pulp cavity
1 0 2 0 0 0 0 0 0 0 0 0 0 0 2 0
Any other fracture (e.g. neck fracture)* 0 0 0 0 0 0 0 0 0 0 0 1 0 0 0 0
Death* 0 0 0 0 0 0 0 0 0 0 0 1 0 0 0 1
No injuries 1 1 1 1 1 0 0 3 1 1 1 0 19 1 0 0
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Discussion Our findings confirm the low selectivity and efficiency of cage-traps to capture foxes in
Spain, reported in previous studies (Herranz 2000; Duarte and Vargas 2001; Muñoz-
Igualada et al. 2008), and for other canids in North America (Way et al. 2002; Shivik et
al. 2005). The Collarum device has been reported as highly selective to catch canids; up
to 100% of selectivity in some areas (Shivik et al. 2000, 2005; Muñoz-Igualada et al.
2008; Junta de Andalucía 2010). Our results are partly in agreement with this, since
only foxes were captured in one of the study sites (100% selectivity), but in the other
one a wild boar was caught (50% selectivity).
Effects of cage-trap type, bait type and scent attractants on efficiency and
selectivity
Our results show that, although cage-traps captured foxes with both baits, live baits
increased their efficiency. This is in agreement with the only study that had previously
tested for differences in efficiency of cage traps to capture foxes using both baits
(Herranz 2000). This increase in fox captures was even more noticeable when live bait
was combined with fox urine as scent attractant. This is not surprising as urine is used
by foxes for scent marking, and plays an important role in olfactory communication and
territoriality (Macdonald 1979; Arnold et al. 2011). However, Monterroso et al. (2011)
observed that captive foxes showed more interest in other attractants than in the urine of
their conspecifics, and this together with the low number of foxes captured in this study
suggest that further works are needed to confirm our finding.
According to our results, the capture rate of non-target species differed between cage-
trap types; it was lower using CT01 and CT02 models than using CT03 (see Appendix
A), likely because the former were smaller in size, which could deter carnivores to enter
inside the trap (Shivik et al. 2005). In addition, CT03 cage-trap type has the bait
chamber in a central position, while the others present a chamber annexed to one side of
the trap. This difference might also explain the increased capture rate observed for
CT03 cage-trap.
Non-target species were captured using both baits and all scent attractants, excepting
COLL. Previous works conducted in Spain have shown that cage-traps baited with live
animals capture higher numbers of non-target species, especially mammalian carnivores
and raptors (Herranz 2000; Duarte and Vargas 2001; Muñoz-Igualada et al. 2008).
82
Similarly, in our study more non-target wild predators were captured using live bait
(13.61 captures/1000 trap-nights) than dead bait (6.48 captures/1000 trap-nights). We
observed a reduction in the capture rate of non-target species using VAL as attractant,
which could be related to the avoidance behaviour of competitors (Harrington et al.
2009). Nevertheless, it could also increase the captures of some felids of conservation
concern (Jerosch et al. 2010; Monterroso et al. 2011); in fact, we captured a European
wildcat using this attractant.
Cage-traps versus Collarum
Cage-traps using baits have been reported as an effective method to capture foxes and
medium-sized canids, such as coyotes (Baker 1998; Baker 2001; Way 2012), but no
information of non-target captures is reported in these studies. In contrast, professional
trappers of France preferred using cage-traps to catch medium-sized mustelids,
considering other methods more efficient to capture foxes (Ruette et al. 2003). Our
results showed how the efficiency and selectivity of cage-traps for foxes may be
improved combining baits and attractants; however, the capture rate of non-target
species remains high compared to Collarum, which showed an acceptable efficiency to
catch foxes.
The Collarum may constitute a good alternative to other predator control methods, such
as cage-traps, passive neck-snares, leg-snares, leg-hold traps, or foothold-traps, which
are less selective regardless of their efficiency (Travaini 1996; Fleming et al. 1998; Way
et al. 2002; Shivik et al. 2005; Muñoz-Igualada et al., 2008, 2010; Duarte et al. 2012).
Although we captured one wild boar using the Collarum device, the selectivity and
efficiency of this trap to capture foxes were acceptabl e, which agrees with previous
studies (Shivik et al. 2000, 2005; Muñoz-Igualada et al. 2008). To our knowledge, we
reported the first case in the literature of a non-canid species captured using this device,
which could be explained by the high density of wild boar in the study area.
Injures to captured animals
We recorded only non-severe injuries during cage-trapping, as those observed in other
studies (Way et al. 2002; Shivik et al. 2005; Muñoz-Igualada et al. 2008). Therefore,
our findings suggest that cage-trapping produces minimal impact on the welfare of
target animals trapped. Way (2012) recently proposed cage-trapping as an alternative
83
method to other unpopular devices to capture canids, such as foot traps, which typically
cause significant injuries to captured animals. Nevertheless, cage-traps must be revised
daily to assure a low level of injuries (Duarte and Vargas 2001). Injuries in non-target
species were even lower than those observed in foxes, and only an azure magpie died in
a cage-trap strangled by the guillotine-door, although this was apparently a highly
unlikely event.
Previous studies reported that 80% of the canids captured with Collarum devices
showed no injuries (Shivik et al. 2000, 2005; Muñoz-Igualada et al. 2008), which is a
percentaje lower than that obtained using other devices, such as cage-traps or leg-traps
(Muñoz-Igualada et al. 2008). Our results are in concordance with this, since the three
foxes captured with this device showed minor injuries, which were caused when they
bit the device. These injuries could be reduced simply by rubber coating the snare. In
contrast, the wild boar captured died likely because the diameter of the loop, designed
for the neck of foxes, is too small for a wild boar neck.
Management Implications
Several studies have shown that cage-traps present a low efficiency and selectivity for
catching wild canids (Duarte and Vargas 2001; Shivik et al. 2005; Muñoz-Igualada et
al. 2008). Our results show how the combined use of live baits and scent attractants may
improve their efficiency to capture red foxes and slightly increase their selectivity in
central Spain. Nevertheless, this cannot prevent the capture of non-target protected
species and selectivity levels obtained are still low (max.21%; see Appendix 3.2.). The
selectivity of this trap depends ultimately on the willingness of gamekeepers or hunters
to release captured non-target animals. Accordingly, we do not recommended the use of
cage-traps for fox management in hunting estates within central Spain. However, the
small sample size obtained in our study requires that more tests are carried out at both
levels, traps design (e.g. mesh size, triggered systems, doors modifications) and the
study of other attractants for target species and/or aversive for non-target species. The
Collarum device can be an alternative to cage-traps since it is effective to catch foxes
and highly selective. Our results suggest also that some minor modification can
decrease the level of harm caused by this device during the capture To our knowledge,
the Collarum device has not been tested yet in areas of continuous presence and high
abundance of large threatened carnivores, such as the Iberian lynx (Lynx pardinus),
84
Iberian wolf (Canis lupus signatus) or brown bear (Ursus arctos). So, it is unknown
whether these species can be captured by this type of trap. Therefore, its use should be
forbidden in these areas at least until more information is gathered. The use of this new
device should be carried out only by skilled technical personnel to ensure proper
handling of trapped animals and always under strict supervision of the competent
authorities in wildlife. Moreover, it is essential that traps are checked at least daily to
avoid injuries and unnecessary animal suffering.
Acknowledgements This study was funded by Consejería de Medio Ambiente of Junta de Comunidades de
Castilla-La Mancha (projects 02-227/RN-52 and PREG-05-23). Special thanks go to
landowners who facilitated the access to the private game estates, and to the field staff
of the regional government of Castilla-La Mancha. Thanks to people who assisted us
during the fieldwork, especially to S. Luna and L.E. Mínguez. We are indebted to O.
Rodríguez, M. Reglero and R. Sobrino who examined the captured animals.
Ethical standards This work was performed in compliance with current Spanish legislation, and follows
the European Union’s recommendations regarding animal welfare. All procedures were
carried out with appropriate permits, provided by the concerned institutions.
85
CAPÍTULO 4: Experimental evaluation of live cage-traps for Black-billed magpies Pica pica management in Spain
Este capítulo ha sido publicado en revista SCI:
Díaz-Ruiz F, García JT, Pérez-Rodríguez L, Ferreras P (2010) Experimental evaluation of live cage-traps for Black-billed magpies Pica pica management in Spain. European Journal of Wildlife Research 56: 239-248.
86
Abstract Black billed magpies (Pica pica) are considered as a nest predator of game and non-
game birds in Europe. In rural areas of Spain magpie control is commonly used as a
management tool in small game hunting estates. Cage-traps with a magpie as a decoy
are the legal method most commonly used for controlling magpies in Spain although its
performance has not yet been experimentally tested. We evaluated the selectivity,
efficiency and the effect of different factors on capture rate of these traps for magpie
control and determine the effect of magpie removal on magpie density. Only 4 out of
197 captures corresponded to non-target species, which were released unharmed. Since
the release of non-target captures depends on the daily checking of the trap and the
trapper commitment, in order to guarantee the efficiency and selectivity of this method
traps should be revised daily by full time, qualified trappers. The efficiency of this
method is high during the breeding season, reducing magpie density in the area where
the control is performed. Highest capture rates were obtained in the first days after cage-
traps setting. Neither the gender nor the origin (local or foreign) of the decoy
significantly affected the capture rate. Among male decoys, experimentally increased
testosterone levels did not increase capture rates. According to our results, the tested
cage-traps with a living decoy could be employed as an efficient and selective method
for magpie population management in Spain, when used by full time, qualified trappers.
Keywords: cage-traps, capture rate, black-billed magpie, selectivity, predator
management.
87
Introduction The effect of predators on species with high socio-economic value frequently causes
conflicts among social stakeholders (Thirgood et al. 2000; Sillero-Zubiri and Laurenson
2001). Such conflicts have often caused the persecution of predators through illegal and
non-selective methods (Delibes-Mateos 2006), causing negative impacts on wildlife
conservation (Villafuerte et al. 1998).
Hunting of red-legged partridges (Alectoris rufa) is an activity of economic interest in
many rural areas of central and southern Spain (Bernabeu 2000). Predation is regarded
in many of these areas as one of the main causes of the partridge populations decline
(Vargas 2002). Among the predators of red-legged partridges, corvids are assumed to
have high impact on partridge nests (Yanes et al. 1998) and, consequently, they have
been traditionally controlled. In these areas, the black-billed magpie (Pica pica) is the
most abundant corvid species, and magpie control is commonly employed in small
game hunting estates in Spain (Otero 1995).
The black-billed magpie is a generalist species, living in a wide range of habitats
(Birkhead 1991). It feeds on a broad spectrum of food types: seeds, fruits, ground
invertebrates, carrion and small vertebrates. Eggs form only a small proportion of the
magpie diet (Birkhead 1991; Martínez 1992), and the impact of magpies on bird
populations is still controversial (Gooch 1991; Thomson et al. 1998; Chiron and Julliard
2007).
Some studies performed in Spain during the red-legged partridge breeding period
suggested that most eggs consumed by magpies belong to red-legged partridges (77.8
%, Herranz 2000). According to artificial nest experiments, magpies may be locally the
most important predator of red-legged partridge nests, (Blanco-Aguiar et al. 2001) and
magpie abundance may be regionally the best indicator of nest predation probability
(Ferreras et al. 2006). Population dynamics of partridges can be negatively affected by
nest predation (Potts 1980), and hence in places where magpies reach high densities,
their removal may increase the breeding success of red-legged partridges and other
game bird species (Martínez de Castilla and Martínez 2004).
Black-billed magpies are in expansion in Europe since 1960 (Birkhead 1991) and a
positive trend of 25% has been reported in Spain between 1995 and 2001
(SEO/BirdLife 2002). Effective management tools for abundant populations of magpies
88
can be therefore necessary for alleviating their pressure on declining species such as
red-legged partridges in circumstances where predation on nests is particularly high.
Many methods have been traditionally used in Spain for capturing magpies, including
currently forbidden methods such as eagle owls (Bubo bubo) as decoys combined with
mist-nests (Wang and Trost 2000), glued-branches (Boza 2002) or poisoned baits, the
latter frequently used in Spain over the last decades (Hernandez and Margalida 2009)
and legally prohibited since 1989 (Law 4 / 1989 on Conservation of Natural Areas and
Flora and Wildlife) to be massive and non-selective methods.
Currently, the methods legally employed for capturing magpies include shooting in
communal roosts or driven hunting, nest destruction and cage-traps. Among these, cage-
traps with a magpie as a decoy is the most commonly used method, likely due to their
efficiency and their ease to operate. Gamekeepers, hunters and manufacturers assure
that cage-traps with a magpie as a decoy are an effective and selective method for
reducing magpie density. Popular recommendations for increasing the capture rate
based on non-systematic observations include using foreign magpies (i.e., magpies
originating from an area different from the one in which cages are being used) as
decoys, and using them throughout the magpie breeding season. Also, these popular
recommendations suggest to use male birds as decoys, as it is expected that their more
active territorial behaviour, which is highly determined by testosterone levels
(Wingfield et al. 1987), will be more effective in attracting conspecifics to traps.
However, no experimental studies have tested these recommendations. On the other
hand, conservationists claim that cage-traps aimed to capture magpies are often not
selective and may negatively affect other species, particularly raptors, which enter into
the traps trying to capture the decoy.
The objectives of the present study were: 1) to assess the selectivity of cage traps, 2) to
evaluate the efficiency of cage traps with a living decoy to capture black-billed magpies,
3) to determine the effect on the capture rate of several factors such as the gender and
testosterone levels of decoys, the origin of decoys, the trapping season and the
permanence time of traps in the same place and 4) to determine the effect of magpie
removal on magpie density.
89
Materials and Methods Study Area
The study was carried out in two hunting estates located in Castilla-La Mancha (Central
Spain) during spring and autumn 2006. Area 1 (960 ha) was placed in the province of
Ciudad Real, within an agricultural-dominated landscape. Natural vegetation layers
were primarily bushes and some trees associated to riparian areas. Hunting is an
important activity in this area, where the main game species are the Iberian hare (Lepus
granatensis), the wild rabbit (Oryctolagus cuniculus) and the red-legged partridge.
Magpies were not systematically controlled before the study, although they were
occasionally shot during the hunting season. Area 2 (547 ha), located in the province of
Toledo, was also dominated by agricultural landscape, and bushes and some trees were
associated with hedgerows. The main game species were the Iberian hare and the wild
rabbit; the density of the red legged partridge was low and hence it was not among the
main game species. Magpies were not controlled in this study area previous to this
study. Magpie density before the breeding season was similar in the two study areas
(see below).
Magpie trapping
We evaluated the efficiency of four different models of cage traps commonly used in
Spain for capturing magpies, all of them using a live magpie as decoy. Cage-traps have
one central chamber for the decoy and several capture chambers around the decoy
chamber, employing a guillotine-type door as capture system. Models 1-3 had four
capture chambers, octagonal prism structure and similar size (approximately: 85 x 85 x
35 cm long x wide x high; See Appendix). Model 4 had two capture chambers and
rectangular prism structure (model 4, 90 x 30 x 30 cm long x wide x high; See
Appendix 4.1.). All cage-traps were made of metallic mesh of variable gauge: thick (3
mm) in model 1, medium (1.9 mm) in model 3 and light (1 mm) in models 2 and 4.
Cage-traps were located near magpie nests (<50 m). For this purpose, nests were
searched previous to the spring trapping experiments (February-March). Magpie nests
are easily found during this season because deciduous trees lack leaves, magpie nests
are large, distinctive and conspicuous (Birkhead 1991), and pairs are very active
building and defending the nest. Traps were separated at least 50 meters among them,
and under tree or shrub shade to avoid sunstroke of the decoy and captured animals in
90
the central hours of the day. All cage-traps were checked daily in the morning, all
captures removed, and the decoy was provided with food and water ad libitum.
In order to compare the effect of different factors on traps performance we defined
capture-rate as the average number of magpies captured per day that a trap is operative
(International Organization for Standardization 1999).
Testosterone manipulation
Testosterone causes aggressive and territorial behaviour in male birds (Wingfield et al.
1987), which could affect the capture efficiency of decoys. For this reason, ten male
decoys, sexed through molecular techniques from blood samples (Fridolfsson and
Ellegren 1999), were experimentally provided with testosterone implants. Implants
consisted in 10 mm long silastic tubes (inner diameter of 1.47 mm, outer diameter of
1.97 mm) filled with crystallized testosterone (T-males; ICN Biomedicals, Irvine, CA)
or empty (C-males). These tubes were sub-cutaneously implanted in the dorsal zone
between the wings (Blas et al. 2006).To assess the efficiency of testosterone implants in
creating significant differences in testosterone levels between T-males and C-males, we
collected 0.3ml of blood from the brachial vein of all birds before and 5 days after
implantation. Blood samples were stored cold (4ºC) and centrifuged within 4 hours, and
plasma was subsequently stored at -80ºC until testosterone quantification. Plasma
testosterone concentration was measured using a commercially available testosterone
enzyme immunoassay (Elisa Kit EIA-1559 from DRG Diagnostics, Marburg,
Germany). Before implanting, C- and T- males did not differ in plasma testosterone
levels (t-test, t=0.87, p=0.39). However, after implanting, T-males showed higher
testosterone levels than C-males (2.3±0.11 (SE) and 1.04±0.13 (SE) ng/ml, respectively;
t-test, t=8.53, p<0.05). Testosterone levels of T-males after implantation were within the
range found in control birds or all birds before manipulation. Although testosterone
levels where not measured again during the rest of the experiment, our previous
experiences indicate that implants of this size are fully active during at least 50 days. In
addition, the visual inspection of implants through the skin indicated that they were still
active (i.e. they were partially filled with testosterone) during the whole extension of the
experiment.
91
Experimental design
Four experiments were designed to test the effect of different factors on capture-rate
(Table 4.1.). Experiments 1, 2 and 4 consisted of n (2-4) blocks or groups of traps of the
same model. Each block included one trap of each treatment. For instance, each block in
experiment 1 consisted of one trap with female decoy, one trap with T-male decoy and
one trap with C-male decoy. Experiment 3 consisted in a single block of 9 traps of
models 1, 2 and 3 (all with 4 capture chambers). Traps belonging to one block were set
in the same area separated at least 50 m.
- Experiment 1 was performed during spring in Area 1, using three decoy types: females
(F), control males (CM) and males implanted with testosterone (TM). All decoys were
from foreign origin. Fifteen cage-traps were installed and remained active for 13 days.
The following variables were evaluated with this experiment: trap model, gender and
testosterone of decoy and days since trap placement. Moreover, the effect of magpie
removals on magpie density was examined together with data from experiments 2 and
4.
- Experiment 2 was performed during spring in Area 1, using F and CM decoys with
different origins, local (L) and foreign (F). Sixteen cage-traps were installed and
remained active 10 days. In this experiment we evaluated the following variables: trap
model, gender and origin of decoys and days since trap placement. Moreover, the effect
of magpie removal on magpie density was examined together with data from
experiments 1 and 4.
- Experiment 3 was performed during autumn in Area 1, using F and CM decoys, all
from local origin. We installed 9 cage-traps that remain active 20 days. This experiment
was used for evaluating trapping season, together with experiments 1 and 2.
- Experiment 4 was performed during the spring season in Area 2, using three types of
decoy: F, CM and TM, all decoys from foreign origin. We installed 12 cage-traps that
remained active during14 days. In this experiment we evaluated trap model, the gender
and testosterone of decoy. Moreover, the effect of magpie removal on magpie density
was examined together with data from experiments 1 and 2.
92
Table 4.1. Summary of field experiments: variables evaluated, decoy gender and testosterone
level (F: female, CM: control male, TM: testosterone implanted male), decoy origin, area where
the experiment was carried out, season, total number of traps employed and duration (days) of
the experiment.
Experiment Variables Decoy
gender & testos.
Decoy origin
Study Area Season
Nr Traps
Duration (days)
Exp.1
Gender and
Testosterone and
trap model
F, CM &
TM Foreign Area 1 Spring 15 13
Exp.2 Gender, origin
and trap model F & CM
Foreign
& Local Area 1 Spring 16 10
Exp.3 Season F & CM Local Area 1 Autumn 9 20
Exp.4
Gender and
testosterone and
trap model
F, CM &
TM Foreign Area 2 Spring 12 14
Handling of captures
Captured animals were examined for possible trap-related injuries. Non-target species
were checked for injuries and released in the capture site. Trap selectivity was defined
as the proportion of captured magpies in relation to the total number (target and non-
target) of captured animals (International Organization for Standardization 1999). The
captured magpies were euthanized through an intraperitoneal injection of sodium
pentobarbitone (200 mg/ml Dolethal Vetoquinol), as recommended for birds (Close et
al. 1997). Data from necropsy of captured magpies (age, gender, physical condition)
were used for further studies (authors in prep.). Some captured magpies were kept alive
and used as decoys in further experiments, once sexed through molecular techniques
from blood samples (Fridolfsson and Ellegren 1999). Those magpies used as decoys in
the same study area where they were captured were considered as “local decoys”,
whereas those captured elsewhere were considered as “foreign decoys”.
Magpie density estimation
The density of magpies in both study areas was estimated with the distance-sampling
method (Burnham et al. 1980), which has been successfully employed to estimate the
density of a number of bird species, including magpies (Newson et al. 2008). We
93
employed the Fourier series estimator as detection function. Surveys were carried out
once a week during the trapping period, following a fixed route (21 km in Area 1 and 12
km in Area 2) with high visibility, starting two hours after sunrise. We indirectly
assessed the effect of magpie removal on population density (experiment 1 and 2, in
study area 1 and experiment 4 in study area 2) by relating the changes in the density of
magpies with the number of animals captured in our cage-traps. Raptor and corvid
species observed during line transects were recorded in order to assess the abundance of
potential magpie predators or competitors which could enter the traps attracted by the
magpie decoy, and related to trap selectivity.
Data analysis
We first modelled daily capture rate (number of magpies trapped each day that a trap
was active) using data from both study areas during spring (exps.1, 2 and 4). Fixed
factors included in this model were: number of days since the trap was installed and
decoy origin (local or foreign). Study area, experimental block and trap location (a
categorical variable identifying each trap position) were included as random effects.
Trap location was nested within experimental block, because these random effects are
not independent. Generalized mixed models with a Poisson error term and a log link
function were used for this and for the remaining analyses of factors affecting capture
rate (see below).
Since the amount of time each cage trap was active differed among experiments (see
Table 4.1.) and capture rate was significantly affected by time since trap installation
(see results), we only considered in further analyses of spring data the captures obtained
during the first 5 days after trap installation, when highest capture rates were obtained
(see results). By this way, we controlled for experiment duration and did not include
this variable in further models of spring data. In order to test for variation in capture rate
among experimental treatments, we modelled the number of magpie captures in the first
5 days after trap installation, using data from spring experiments (exps. 1, 2 and 4), and
the following explanatory factors: trap model (a categorical factor with four levels),
type of decoy (female, Control-male and Testosterone-male), decoy origin (local or
foreign) and study area (1 or 2). Models were fitted to all the data from experiments 1, 2
and 4. We ranked the obtained models according to their Akaike Information Criterion
value (AIC) with respect to the principle of parsimony (Akaike 1973; Burnham and
94
Anderson 1998). The statistical significance of the parameters estimated was assessed
using the Wald test.
Finally, the effect of season on capture rate was analysed including only data from study
area 1, where trapping was performed both in spring (experiments 1 and 2) and in
autumn (experiment 3). Since the decay of capture rate along time since trap installation
could differ between seasons, we considered the daily capture rate as dependent
variable, and fitted generalized linear models to these data, including day since trap
installation, season and their interaction as fixed effects.
Results Selectivity
A total effort of 708 trap-days during spring and autumn 2006 produced the capture of
193 magpies and 4 individuals of non-target species, which indicate a high selectivity of
the trapping method (97.9% captures of the target species). Non-target captures were:
common buzzard (Buteo buteo), genet (Genetta genetta), Western hedgehog (Erinaceus
europaeus) and red-legged partridge. None of these captured animals resulted injured
and they were released in the capture site. Despite the low capture rate of non-target
species, several medium raptors, potential predators of magpies, were frequently seen in
the surroundings (<100 m) of the traps during the daily checks and during the weekly
transects for magpie density estimation (Table 4.2.).
Effect of trapping time on capture rate
Average capture rate during spring was 0.32 magpies/trap-days (see Table 4.3.). We
checked for overdispersion in the data, and extra-dispersion scale was close to 1 (0.9),
therefore it was not necessary to correct for this factor and the use of Poisson errors was
appropriate for modelling capture rates. Capture rate significantly decreased over time
since trap installation (Table 4.4.; Figure 4.1.). Other significant term included in the
models was the interaction between time and decoy origin (see Table 4.4.). According
to this, local decoys provided higher capture rate than foreign decoys during the first
days, but lower during latter days (Figure 4.2.). Study area, block and trap location,
included as random terms, did not result significant.
95
Table 4.2. Non-target species susceptible of being captured in the traps that were observed in
the traps vicinity during daily trap checking and along weekly linear transects in both study
areas.
Linear transects Trap vicinity
Area 1 Area 2 Area 1 Area 2
Circus sp. 7 6 7 0
Buteo buteo 6 13 4 1
Asio otus 0 0 1 0
Milvus migrans 6 0 0 0
Accipiter nisus 2 0 0 0
Hieraaetus pennatus 1 0 0 0
Corvus corone 0 0 1 0
Corvus monedula 36 108 0 0
Total length 219 km 60 km
Table 4.3. Number of magpies captured, trapping effort and average capture rate during spring
and autumn in each study site.
Season Site Nr magpies
captured
Effort
(trap-days)
Capture rate
Site Average
Spring Area 1 105 355 0,26
0.32 Area 2 62 168 0,37
Autumn Area 1 26 185 0.14
96
Table 4.4. Summary of results of the mixed model of capture rate including time since
installation and decoy origin (data from spring in study areas 1 and 2). Area, block and
trap location are controlled as random variables.
Effect DF F P
Time since installation 1,536 46.56 0.0001
Decoy origin 1,305 3.54 0.061
Time x decoy origin 1,536 4.74 0.030
Figure 4.1. Daily capture rate changes along time since trap installation during spring 2006
(experiment 1 and 2) and autumn 2006 (experiment 3) in area 1.
97
Figure 4.2. Expected capture rate as a function of time since trap installation (days) and the
origin of the magpie employed as decoy.
Effects of type of decoy and trap model on capture rate during spring
The following analysis focused on the number of magpies captured during the first five
days after trap installation, when capture rate is highest in all the experiments (see
Figures 4.1. and 4.2.). None of the factors considered (trap type, gender-testosterone and
decoy origin) resulted significant in the models (Table 4.5.). However trap type was
included in the five models with lowest AIC and had the highest sum of Akaike weight
(Tables 4.5. and 4.6.). The trap types with four capture chambers tend to have higher
capture rates than the model with two capture chambers (Figure 4.3.).
Effect of season
Average capture rate in study area 1 during autumn (experiment 3) was lower (0.14
magpies/trap-day) than during spring (0.26 magpie/trap-day; see Table 4.3.; Figure
4.1.). However, only days since trap installation, but not season, resulted significant in
generalized models including data from spring and autumn in study area 1 (Table 4.7. ).
98
Table 4.5. Significance of variables used in the mixed models for magpies captured during the
five days since trap installation. Last column indicates the relative importance of each predictor
variable estimated as the sum of the Akaike weights over all the models including each variable.
Variable
Degr. of
freedom Wald test p Σwi
Intercept 1 0.531 0.466
Trap type 3 0.992 0.609 0.618
Gender & testosterone 2 3.433 0.180 0.275
Origin 1 2.407 0.121 0.209
Table 4.6. Summary of mixed models for magpies captured during the five days since trap
installation. Variables: Tr: trap type; DS: decoy gender and testosterone level; DO: decoy
origin.
Model Variables Degr. of
freedom AIC ∆AIC Chi-2 p wi
1 Tr 2 172.219 0.000 3.886 0.143 0.106
2 Tr + DO*Tr 4 172.648 0.430 7.456 0.114 0.086
3 DO 1 173.211 0.992 0.893 0.345 0.065
4 Tr + DS*DO 4 173.508 1.289 6.597 0.159 0.056
5 DS*DO 2 173.587 1.368 2.518 0.284 0.054
6 DO + Tr 3 173.704 1.485 4.401 0.221 0.051
7 DO*Tr 2 173.850 1.631 2.254 0.324 0.047
8 DS 2 173.926 1.707 2.178 0.336 0.045
9 Tr + DS*DO + DO*Tr 6 174.075 1.856 10.030 0.123 0.042
99
Figure 4.3. Average number (±SE) of captured magpies per trap during the first 5 days after
trap installation according to trap model (1-3, with four capture chambers; 4 with two capture
chambers).
Table 4.7. Summary of results of the mixed model of capture rate including time since
installation and season (only data from study area 1).
Effect of captures on magpie density
Magpie density before the breeding season was estimated as 0.23±0.06 magpies/ha in
study area 1 and 0.39±0.09 magpies/ha in study area 2. The magpies removal during the
breeding season (spring) was followed by a decline in magpie density in both study
areas (see Figure 4.4.). In area 1 the initial density declined coinciding with the first 60
Variable Degr.
of freedom
Wald test p Σwi
Intercept 1 0.223 0.637
Season 1 2.194 0.139 0.378
Time since installation 1 13.017 0.0003 1.000
Season x Time since installation 1 2.054 0.152 1.175
100
magpies removed. Despite magpie density increased in the fourth census, the density at
the end of the trapping season was lower than the initial density (Figure 4.4a.). After the
trapping ceased, magpie density tended to increase. In area 2, the effect of trapping is
clearer than in area 1. There, the initial density of magpies was reduced following the
trapping season (Figure 4.4b.), and did not increase after the end of the trapping season.
Figure 4.4. Changes in magpie density (magpies/ha ± SE) along time (dashed line) and
accumulated captures during the trapping season (solid line) in study area 1 (A) and study area 2
(B).
101
Discussion The tested traps are highly selective for the capture of magpies, according to our results
(97% selectivity). This is not the result of the absence of species susceptible to be
captured in the traps. Both systematic and non-systematic surveys indicate that species
susceptible to enter the traps are abundant in the study areas (see Table 4.2.). This is the
case of magpie predators, such as medium-size raptors, and magpie competitors, such as
other corvids (e.g. jackdaw (Corvus monedula); Högstedt 1980). Only a common
buzzard was captured in the traps among the medium-size raptors able to capture
magpies that were observed Accipiter nisus, Circus sp., Buteo buteo. However, we did
not detect in any of the study areas the presence of goshawk (Accipiter gentilis), a
reputed magpie predator (Mañosa 1994), which likely would enter the traps. Some
small carnivores Genetta genetta, Martes foina, Mustela nivalis, and Mustela putorius
which could be attracted by the decoy and captured in these traps, are likely present in
the study areas according to distribution atlas (Palomo et al. 2007), although we lack
quantitative data on their abundance. However, only a common genet was captured
during the study.
The release of non-target animals captured in magpie traps, when used as a management
tool, depends totally on the trapper commitment, as it happens with other traps used for
predator control (Duarte et al. 2001). Because of that, the training and the awareness of
the trappers are necessary to guarantee the release of non-target captures. Traps must be
checked daily to prevent long restraint periods which can reduce the animal welfare and
eventually cause the death of both target and non-target species.
The assessed traps resulted highly effective for the capture of magpies during the
breeding season, producing an average capture rate of 0.32 magpies/trap and day. The
daily capture rate was highest during the first day after trap installation (0.73-0.87
magpies/trap; Figure 4.1.). These values are much higher than those obtained in one-day
attempts with bal-chatri traps using an adult female as decoy (0.43; Wang and Trost
2000), although other factors such as magpie density could have affected capture rate.
The trap type was included in the best models of capture rate during the first five days,
although it was not a significant term. In fact, number of capture chambers seems to
increase the capture rate (although not significantly), since trap models with four
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chambers tended to provide more captures than the model with two capture chambers
(Figure 4.3.).
The popular recommendation of using foreign magpies as decoys to increase captures is
not supported by our data, since the origin of the decoy seems not to affect the capture
rate. In fact, we obtained a similar number of captures when using the first magpie
captured as decoy in the trap where it was captured (authors unpublished, data not
included). Although both magpie males and females defend territories, this behaviour is
more conspicuous in males (Baeyens 1981; Birkhead 1991). However, neither the
gender of the decoy nor the testosterone level affected significantly the capture rate
(Table 4.5.). Therefore, our data do not support the popular assumption about increasing
captures by using male decoys from distant populations.
The lower capture rate in autumn compared to spring (Table 4.3.) could be explained, at
least partially, by the lower density just before autumn trapping period (0.17 and 0.23
magpies/ha, respectively for autumn and spring in study area 1). This lower density in
autumn is probably a result of the magpies removed during the experimental trapping in
spring. Also during autumn and winter, magpies are more sociable and not so
aggressive when defending their territory (Eden 1989; Birkhead 1991). This lower
territoriality during the non-breeding season can also explain the lower tendency of
magpies to enter the traps.
Recent studies show that predator control often do not reduce local predator abundances
(Baker and Harris 2006; Beja et al. 2009). However, in our study, there was a strong
decline in one area, whereas in the other the pattern was unclear (Figure 4.4.). In the
study area 2 we observed an increase in magpie density one week after trapping started,
which was followed by a density decrease during the next week (Figure 4.4b.). In both
areas, these density fluctuations are probably due to sampling variability.
In any case, in both study areas trapping was able to reduce magpie density during the
breeding season of game species such as red-legged partridge and therefore the potential
predation impact upon nests reduced.
Management Implications
The use of non-selective, illegal methods for predator control in Spain is one of the
main causes of mortality for many predator species, both mammals and birds, some of
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them endangered (Villafuerte et al. 1998). Therefore, it is necessary to identify selective
methods for predator control to be used as management and conservation tools in
particular situations of high abundance of generalist, non-protected predators. Such is
the case of the traps tested in the present study, which have resulted highly selective and
efficient. Some recommendations for using this type of traps for managing magpie
populations can be drawn from our results. The breeding season is the most appropriate
for effectively control magpie populations with these traps, since capture rate is higher
in this period, the magpie density of unmanaged populations is lowest just before
breeding and easier to be controlled. On the other hand, this period coincides with
nesting of most bird species, including red-legged partridges, reducing in this way nest
losses due to magpie predation. Traps located in the proximity of magpie nests are
highly effective but their efficiency would increase if they are moved to a new location
after 4-5 days. Either local or foreign magpies of any gender can be used as decoys in
the traps with similar results in capture rate. Traps should be checked daily in order to
avoid the reduction of welfare of captures and the personnel in charge of setting and
manipulating these traps must be encouraged to liberate individuals of non-target
species. Other likely side effects of the traps assessed should be considered before their
generalized use. For instance, the effect of the reduction of magpie populations on Great
spotted cuckoo populations (Clamator glandarius), a nest parasite specialized on
magpie nests (Soler et al. 1996), should be scientifically evaluated and taken into
account when authorising the use of traps for magpie control.
Acknowledgements This study was funded by Consejería de Medio Ambiente of Junta de Comunidades de
Castilla-La Mancha (project PREG-05-23). Patrick Fasolo kindly provided the first
magpie decoys to start the trapping experiments, and shared with us his long experience
with the use of the traps. Land owners and game owners of both study areas facilitated
the access to estates and facilitated the field tests. Salvador Luna performed most of the
field work. Luis Enrique Mínguez kindly assisted in the field work and solved most
bureaucracy during the project development. Beatriz Arroyo provided helpful support
with the statistical analyses.
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Ethical standards All the experiments comply with the current Spanish laws, and were performed with the
corresponding legal authorizations and following current guidelines for animal welfare.
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CAPÍTULO 5: Assessing the influence of predator control on target and non-target predator populations using occupancy models
Este capítulo se encuentra en preparación para ser enviado a una revista SCI:
Díaz-Ruiz F, Caro J, Delibes-Mateos M, Arroyo B, Ferreras P (en preparación) Assessing the influence of predator control on target and non-target predator populations using occupancy models.
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Abstract
Lethal control of predators may affect the structure and composition of predator
communities, and this can have far-reaching ecological consequences, including the
precipitation of trophic cascades and species declines. Understanding the effects of
predator control on predator communities is therefore of great interest for the
conservation and management of wildlife. In the present study, we used camera traps
and occupancy models to assess the influence of red fox (Vulpes vulpes) control on
foxes (target species) and stone marten (Martes foina, non-target species) across 12
localities of Mediterranean environments in central Iberian Peninsula. Our results show
that the intensity of fox control was not associated with red fox occupancy, whereas it
was negatively related to red fox detectability. This suggests that fox control could
decrease the species’ abundance if we assume a relationship between abundance and
detectability as suggested by some authors. On the other hand, the intensity of fox
control was positively related to stone marten occupancy, but unrelated to its
detectability. Nevertheless, habitat composition and prey availability were more closely
associated with site occupancy of both species than red fox control. Our study suggests
that predator control could affect target (red fox) populations both spatially and
numerically, differently than non target (stone marten) populations. Furthermore, red
fox extractions could benefit subordinate sympatric mesocarnivores, such as stone
marten, through a competitor release process. This work provides valuable information
on the ecological consequences of fox control to be considered in the management of
red fox populations conducted in game estates.
Key words: competitor release, hunting, mesocarnivores, predator management, Vulpes
vulpes, Martes foina
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Introduction Changes in the relative abundance of sympatric carnivores can have far-reaching
ecological consequences, including the precipitation of trophic cascades and species
declines (Prugh et al. 2009; Levi and Willmers 2012). Lethal control of predators may
be one of the main factors affecting the structure and composition of carnivore
communities in areas where this management practice is performed. The main goal of
predator control is reducing the incidence of predation on prey, and it has become a
widely management tool used to preserve both prey species of conservation concern and
human interests (Woodroffe et al. 2005). In this sense, the red fox is the species of
predator most often persecuted because it usually impacts negatively on livestock or
game species (Sillero-Zubiri et al. 2004).
In Spain predator control is mostly focused on the red fox and it is usually carried out
by hunters and game managers (Díaz-Ruiz and Ferreras 2013), who consider it is
indispensable to reduce fox impact on small-game prey (Rios-Saldaña 2010; Delibes-
Mateos et al. 2013). The red fox is a game species in Spain; it is legally culled during
the regular hunting season (autumn-winter, pre-reproduction fox season) mainly by
shooting (Delibes-Mateos et al. 2013). In some small game estates, exceptional permits
are also granted to cull foxes outside the regular hunting season (Delibes-Mateos et al.
2013) by means of traditional methods, such as cage traps and neck snares (Muñoz-
Igualada et al. 2008, 2010).
Although game managers often consider that fox numbers are reduced as a result of
intensive fox culling (but see Delibes-Mateos et al. 2013), the effect of predator control
on fox populations is still controversial, as several studies have shown different, often
opposed, results (Heydon et al. 2000; Baker and Harris 2006; Saunders et al. 2010;
Mateo-Moriones et al. 2012; Berry et al. 2013). Fox control could also have effects on
other sympatric mesocarnivores. On the one hand, the Competitor Release Hypothesis
states that the reduction of a dominant competitor species may benefit other subordinate
competitor that increases its abundance (Caut et al. 2007). This has been shown
experimentally in UK, where the culling of Eurasian badgers (Meles meles), dominant
competitor, was associated with an increase in densities of a subordinate competitor, the
red fox (Trewby et al. 2008). On the other hand, non-selective predator control methods
(e.g. cage-traps, poisoning, etc) are sometimes used in some hunting estates, resulting in
the culling of both target and non-target mesocarnivore species (Duarte and Vargas
108
2001; Barrull et al. 2011). In this sense, recent studies based on theoretical simulation
models indicate that certain levels of non-selective control of red fox populations could
alter the carnivore communities with an increase in the abundance of the target predator
(i.e. the red fox), and a reduction in the numbers of other non-target species (red fox
“competitors”), such as the Eurasian badger, the stone marten (Martes foina) and the
pine marten (Martes martes) (Casanovas et al. 2012; Lozano et al. 2013).
It is therefore of particular interest to all stakeholders involved in the conservation and
management of wildlife to understand the multiple effects of predator control on
terrestrial carnivore communities, including the interactions between carnivore species.
Detecting these effects on the populations of both target and non-target carnivores is not
an easy task because these species are often cryptic and occurs at low densities, and
therefore specific sampling methods are required to a reliable monitoring of their
populations (Boitiani and Fuller 2000; Long et al. 2008). Camera traps constitute a good
alternative to monitor rare, elusive species, such as mammalian carnivores and the effect
of management interventions on carnivore populations (Johnson et al. 2009; Sarmento
et al. 2011; Schuette et al. 2013). Camera-trapping data combined with new
methodologies of statistical analysis allows characterizing the status and changes in the
populations of these species. For example, Occupancy Models are often applied to
camera trapping data to estimate the probability of site occupancy of a species; i.e. the
proportion of sites occupied by the species (MacKenzie et al. 2002; MacKenzie et al.
2006). This is estimated from the detection/non-detection data obtained from several
sampling sites and during several sampling occasions. Occupancy has been used as a
surrogate of abundance for many inferential purposes, including habitat selection,
population dynamics and distribution, or changes in population size (Royle and Nichols
2003; MacKenzie and Nichols 2004; MacKenzie et al. 2006). To obtain unbiased
estimates of occupancy it is fundamental to account for detection probability; i.e. the
probability of detecting the species, given its presence, during the independent survey of
sampling sites (MacKenzie et al. 2002; Mackenzy et al. 2006)
In the present study, we combined the use of camera traps and occupancy models to
assess the influence of red fox control on occupancy and detection probability of
populations of foxes and stone martens, a non-target predator, in Mediterranean
environments within central Iberian Peninsula. In addition, we discuss about the
109
potential relationship between predator control and the abundance and spatial
distribution of both species, and it implications for the predator management.
Material and Methods Study areas
The study was conducted in 12 localities within central Spain (Figure 5.1.),
characterized by hot and dry summers, cold winters and most rainfall occurring during
autumn-spring months (Mediterranean bioclimatic region; Rivas-Martínez et al. 2004).
The landscape was heterogeneous, and the main habitats present in all localities were
Mediterranean scrubland (mainly (Cistus spp.) in combination with holm oak (Quercus
ilex) forests), mixed with cereal croplands and permanent crops, such as olive groves
(Olea europaea) and vineyards (Vitis vinifera), and natural pastures. Other less
abundant habitats included riparian areas and ‘dehesas’ (pastureland with savannah-like
open tree layer, mainly dominated by Mediterranean evergreen oaks). Surface and
habitat composition varied among localities (see Table 5.1. and Appendix 5.1. for a
detailed description).
All localities were hunting estates, with the exception of two protected areas (numbers 5
and 11 in Figure 5.1.), where hunting was not allowed. The main small game species
were European wild rabbit (Oryctolagus cuniculus; hereafter rabbit), red-legged
partridge (Alectoris rufa) and Iberian hare (Lepus granatensis). Red deer (Cervus
elaphus) and wild board (Sus scrofa) were the main big game species. Hunting estates
were managed to boost small game numbers, mainly by the provision of supplementary
food and water, and predator control. The intensity of fox control varied among hunting
estates (Table 5.1., and see below).
Camera trap surveys
We carried out camera trap surveys between 2010 and 2013 in late spring and summer
(May-September, Table 5.1.), after Iberian mesocarnivores breeding season (Blanco
1998). We used two models of infrared-triggered digital cameras: Leaf River IR5 (Leaf
River OutDoor Products, Taylorsville, Mississippi, USA) and HCO ScoutGuard (HCO
OutDoor Products, Norcross, Georgia, USA). Camera stations were regularly deployed
with an average distance of ~1.2 km among neighboring cameras, ensuring
independence between them (Monterroso et al. 2011, 2013). The number of camera
110
traps deployed in each study locality varied from 14 to 20, according to locality surface
(Table 5.1.).
Figure 5.1. Situation of the study localities (1-12) in the Iberian Peninsula.
Cameras were mounted on trees approximately 0.5–1.0 m off the ground and set to
record time and date when triggered. Cameras operated 24 h a day for an average period
of 28.4±0.4 days (mean±SE). We programmed cameras with the minimum time delay
between consecutive photos to maximize the number of photos taken per captured
individual (Monterroso et al. 2011; 2013), so assuring the species identification of each
event.
In order to increase the detection probability of mesocarnivores, we set the sensitivity of
the infrared sensor at the highest level, and used Valerian scent and Iberian lynx (Lynx
pardinus) urine as lures. This combination has been described as an effective attractant
for a wide range of Iberian carnivores (Monterroso et al. 2011). Between 3 and 4 ml of
each lure were put in two independent perforated plastic vials secured to a metal rod.
Lures were set at 2-3 meters from each camera trap, and were replenished every two
weeks, when cameras were inspected to check the batteries and to replace memory
cards. Consecutive images of the same species within 30 min interval were considered
as the same event, unless animals were clearly recognized as different individuals, and
111
those separated by a longer interval as independent events (Kelly and Holub 2008;
Davis et al. 2011; Delibes-Mateos et al. 2014).
Table 5.1. Description of study localities. The predominant landscape (agriculture or
scrubland) is indicated along with the habitat types present in each area: Oa: open areas, Scr:
scrubland, Wc: woody crops, Rip: riparian, Fo: forest, Dh: dehesa. “Red fox control” is the
number of foxes culled per square km and year. “Control Method” is the main method
employed to remove foxes: shooting, snaring or no control (No). “Cameras” indicate the
number of camera-traps used in each locality. “Effort” (survey effort) is expressed as camera-
days, or the sum of days each camera was active in the field in each locality.
Study site
(Map ID)
Area (ha)
Locality type and Uses
Landscape (Habitats
types)
Red fox control (foxes/km2year)
Control Method
Sampling Year Cameras Effort
1 2000 Social hunting estate Small
game
Agricultural (Oa, Scr, Rip, Wc)
0.08 Shoot 2010 20 620
2 1600 Commercial
hunting estate Small game
Scrubland (Oa, Scr,
Rip) 1.98 Snares 2010 15 424
3 5000 Social hunting estate Small
game
Agricultural (Oa, Scr, Rip, Wc)
0.89 Shoot 2011 18 493
4 3580 Social hunting estate Small
game
Agricultural (Oa, Scr, Rip, Wc)
0.43 Shoot 2011 17 485
5 2140 Protected area Conservation
Scrubland (Oa, Scr,
Rip, Dh, Fo) 0 No 2011 19 682
6 1560 Social hunting estate Small
game
Scrubland (Oa, Scr, Rip, Wc)
1.30 Snares 2011 20 645
7 2140 Social hunting
estate Big game
Agricultural (Oa, Scr, Rip, Dh)
0 No 2012 20 495
8 2000 Social hunting estate Small
game
Agricultural (Oa, Scr, Rip, Wc)
4.00 Snares 2012 20 503
9 900 Commercial
hunting estate Big game
Scrubland (Oa, Scr,
Rip, Dh, Fo) 0.10 Shoot/Cage trap 2012 15 417
10 900 Commercial
hunting estate Small game
Agricultural (Oa, Scr,
Rip) 2.70 Snares 2012 14 372
11 2600 Protected area Conservation
Scrubland (Oa, Scr,
Rip) 0 No 2012 20 529
12 1600 Commercial
hunting estate Big game
Scrubland (Oa, Scr,
Rip, Dh, Fo) 0.70 Shoot 2013 18 463
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Selection of covariates
Several factors could influence the probability of site occupancy and detectability of
carnivores. Among these habitat composition and prey availability are the main factors
explaining the presence/absence of carnivores at a given site (Long et al. 2011;
Sarmento et al. 2011; Silva et al. 2013), although human disturbance, including predator
control, may also play an important role (Long et al. 2011).
Fox control data (i.e. human disturbance covariate) were gathered through face-to-face
interviews with game managers of each hunting estate, conduct before field sampling
(at the end of the regular hunting season, in February). We asked managers about the
number of foxes removed in the previous hunting season (Table 5.1.). The intensity of
red fox control (IFC) was estimated as the number of foxes removed per km2 and year
(fox·year-1·km-2), and it was recorder at locality level. We confirmed during the
interviews that the same fox control effort was developed in each locality for at least
two years before our field samplings. Methods employed to control foxes varied
between study localities, including shooting, cage-trapping and neck snaring (Table
5.1.).
We also recorded data of covariates associated with habitat type and prey availability at
each camera site to account for potential heterogeneity in the probability of occupancy
and detectability. We used a Geographic Information System (QGIS version 1.8.0) to
calculate the percentage of each habitat type within a circular buffer of 200-m radius
around each camera trap (Ordeñana et al. 2010; Sarmento et al. 2011; Silva et al. 2013).
We classified habitats into 6 different types using the combination of CORINE land-
cover 2006 (European Environment Agency; http://www.eea.europa.eu), Updated
satellite orthophotos (National Geographic Institute, http://www.ign.es/), and field data
recorded on site during installation-revision of camera traps. Main habitat types were
scrublands (SCR), open areas (OA), woody crops (WC), riparian (RIP) and “dehesa”
(DEH) (Appendix 5.1.). The European rabbit is the main prey of most mesocarnivores
in the Iberian Peninsula (Delibes-Mateos et al. 2008a). Therefore, rabbit availability
(hereafter RA) was assessed for each camera station as the number of independent
detections per 100 trap days and used as a measure of prey availability (Kelly and
Holub 2008; Davis et al. 2011; Monterroso 2013).
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To avoid multicollinearity, we eliminated any covariate highly correlated with other
covariates (Spearman rank correlation≥0.70). Thus, among habitat covariates, we
eliminated OA as it was highly correlated with SCR. Prior to analysis we standardized
all continuous covariates using the z-transformation (MacKenzie et al. 2006).
Occupancy models
We constructed detection histories for each camera trap placed on the 12 study
localities. We divided each survey period into four 1-week sampling occasions during
which the detection/non detection data of each target species was recorded (Sarmento et
al. 2011; Monterroso 2013).
For each species we developed single season occupancy models (MacKenzie et al.
2002) using the software PRESENCE 5.8 (Hines and Mackenzie 2013); these are based
on the assumption that all sampling sites always present the same level of occupancy
(i.e., either occupied or not) during the sampling period (MacKenzie et al. 2002). As our
goal was to estimate the influence of covariates on occupancy and detectability
simultaneously, we followed a two steps process to fit global models, as previously
described (Sarmento et al. 2011; Harihar and Pandav 2012; Monterroso 2013).
In the first step we selected independently the covariates that best explained detection
probability (Habitat and IFC covariates) and occupancy (all covariates). We used a
sequential modeling approach to find the best model for each parameter, by discarding
uninformative variables (Arnold 2010). We first held occupancy (Ψ) constant and
proceeded to find the best detection (p) model. In other words, we started building a full
effect model for detection probability, and performed a backward-stepwise model
selection to sequentially eliminate the covariate with the weaker effect size (β/SE). This
process was kept until the deletion of an additional covariate led to an increase in AICc,
keeping the variables included in the top model (Monterroso 2013). The same process
was developed to find the best occupancy model, holding detection probability constant.
In the second step we built for each species a global model that included all informative
covariates selected in the top models of detection and occupancy probability developed
in the first step. Then we followed the same procedure of backward-stepwise model
selection as described above to find the final model set for each species, we selected as
informative covariates for inference those that were included in models with ∆AICc< 2
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units of the top-supported model (Burnham and Anderson 2002). We estimated overall
AIC weights for individual variables by summing the AIC weights of all the candidate
models in which they were included (Mackenzie et al. 2006). If no single model
accounted for >90 % of the total model weights, we model-averaged by extracting the
top 95 % model confidence set and recalculating model weights (Burnham and
Anderson 2002). Model averaged estimates were calculated using the spreadsheet
developed by B. Mitchell (http://www.uvm.edu/%7Ebmitchel/software.html).
Results Camera-trapping survey
Red fox was detected in all study localities with naïve occupancy (i.e. the raw
proportion of. camera traps where the species was detected) ranging 0.20-0.95, and a
total of 254 positive sampling occasions. Stone marten was detected in more than half
of study localities (n=7, 58%) with a total of 65 positive sampling occasions, and naïve
occupancy ranging 0-0.60. Besides red fox and stone marten, other 5 species of wild
mesocarnivores were detected during the sampling period at different localities:
common genet (Genetta genetta), Egyptian mongoose (Herpestes ichneumon), Eurasian
badger (Meles meles), least weasel (Mustela nivalis) and wildcat (Felis silvestris)
(Appendix 5.2.).
Explanatory covariates of detection and occupancy
According to the sequential modeling approach to select the covariates, the intensity of
fox control was selected as covariate for fox detection to be included in the second step
(Table 5.2.). The scrublands, riparian areas, dehesa, the intensity of fox control and
rabbit availability were selected as covariates for red fox occupancy to be included in
the second step (Table 5.3.).
For the stone marten the proportion of scrubland and the intensity of fox control were
selected for the detection probability (Table 5.2.). The proportion of scrubland, rabbit
availability and the intensity of fox control were selected as covariates for stone marten
occupancy to be included in the second step (Table 5.3.).
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Table 5.2. Models obtained in the process developed for selecting detection covariates, by fitting Ψ constant: Ψ(.), for red fox and stone marten. Selected covariates are those that are included in the top model, which is marked in bold. IFC: intensity of fox control; RIP: % riparian habitat; SCR: % scrubland; WC: % woody crops.
Model AIC ∆AIC AIC wt K 2log L Red fox
Ψ(.), p(IFC) 895.72 0.00 0.436 3 889.72 Ψ(.), p(IFC+RIP) 896.28 0.56 0.330 4 888.28 Ψ(.), p(IFC+RIP+SCR) 897.90 2.18 0.147 5 887.9 Ψ(.), p(IFC+RIP+SCR+WC) 899.60 3.88 0.063 6 887.6 Ψ(.), p(full) 901.60 5.88 0.023 7 887.6 Ψ(.), p(.) 906.45 10.73 0.002 2 902.45
Stone marten Ψ(.), p(IFC+SCR) 421.18 0 0.313 4 413.18
Ψ(.), p(SCR) 421.40 0.22 0.280 3 415.4 Ψ(.), p(IFC+RIP+SCR) 421.50 0.32 0.267 5 411.5 Ψ(.), p(IFC+RIP+SCR+WC) 423.42 2.24 0.102 6 411.42 Ψ(.), p(full) 425.38 4.20 0.038 7 411.38
Table 5.3. Models obtained in the process developed for selecting occupancy covariates, by fitting p constant: p(.), for red fox and stone marten. Selected covariates are those that are included in the top model, which is marked in bold. IFC: intensity of fox control; RIP: % riparian habitat; SCR: % scrubland; WC: % woody crops; DEH: % dehesa; RA: rabbit availability.
Model AIC ∆AIC AIC wt K 2log L Red fox Ψ(SCR+RIP+DEH+IFC+RA), p(.) 904.22 0.00 0.501 7 890.22 Ψ(SCR+RIP+DEH+IFC), p(.) 905.44 1.22 0.272 6 893.44 Ψ(full), p(.) 905.81 1.59 0.226 8 889.81
Stone marten Ψ(SCR+IFC+RA), p(.) 414.06 0.00 0.403 5 404.06
Ψ(SCR+RA), p(.) 415.16 1.10 0.233 4 407.16 Ψ(SCR+RIP+IFC+RA), p(.) 415.33 1.27 0.214 6 403.33 Ψ(SCR+RIP+DEH+IFC+RA), p(.) 416.66 2.60 0.110 7 402.66 Ψ(full), p(.) 418.66 4.60 0.040 8 402.66
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Selection of global models and model averaging
The second step for the red fox produced three models with ∆AICc< 2 (Table 5.4.).
According to the model averaging, the proportion of scrubland, riparian areas and
dehesa as well as rabbit availability and fox control intensity influenced red fox
occupancy probability (Table 5.4.). The three habitat types were the most explicative
covariates (w= 0.99) and were positively associated with occupancy probability; a
marginally significant effect was obtained for the proportion of riparian areas (Table
5.5.; Figure 5.2a.). Rabbit availability was also positively associated with occupancy
probability (Table 5.5.). Although with lower weight of evidence (w= 0.17), red fox
control intensity was negatively related to the probability of red fox occupancy (Table
5.5.; Figure 5.3.). Red fox detection probability was affected negatively by red fox
control intensity (Table 5.5. and Figure 5.2b.), which was included in the three top
models (Table 5.4.).
Table 5.4. Single season occupancy models (top ranked models ∆AIC < 2) for the red fox and stone marten including covariates previously selected for p and Ψ. IFC: intensity of fox control; RIP: % riparian habitat; SCR: % scrubland; DEH: % dehesa; RA: rabbit availability.
Model AIC ∆AIC AIC wt K 2log L Red fox Ψ(SCR+RIP+DEH+RA), p(IFC) 893.73 0.00 0.492 7 879.73 Ψ(SCR+RIP+DEH), p(IFC) 894.61 0.88 0.317 6 882.61 Ψ(SCR+RIP+DEH+RA+IFC), p(IFC) 895.63 1.90 0.190 8 879.63
Stone marten Ψ(SCR+IFC+RA), p(.) 414.06 0.00 0.444 5 404.06
Ψ(SCR+RA), p(.) 415.16 1.10 0.256 4 407.16 Ψ(SCR+IFC+RA), p(SCR) 415.48 1.42 0.218 6 403.48
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Table 5.5. Model averaged coefficients (β) and confidence intervals (CI 95%) of the covariates included in the set of models explaining the red fox and stone marten detectability p and occupancy Ψ. “wt” refers to covariate AIC weights. Habitat covariates: RIP riparian; DEH dehesa and SCR scrubland. IFC: intensity of fox control. RA: rabbit availability. **Significant covariates. *Marginally significant covariate.
Red fox Covariate β CI 95% wt
Ψ
intercept 0.53 (0.18, 0.88) RIP* 0.39 (-0.05, 0.83) 0.99 DEH 0.29 (-0.13, 0.72) 0.99 SCR 0.22 (-0.10, 0.54) 0.99 RA 0.32 (-0.50, 1.14) 0.66 IFC -0.01 (-0.17, 0.15) 0.17
p intercept 0.03 (-0.18, 0.25)
IFC** -0.36 (-0.6, -0.2) 1
Stone marten Covariate β CI 95% wt
Ψ
intercept -1.28 (-2.02, -0.3) SCR** 0.769 (0.14, 1.39) 1.00 RA* -3.84 (-7.72, 0.06) 1.00 IFC 0.28 (-0.25, 0.81) 0.71
p intercept -1.27 (-1.78, -0.75)
SCR 0.04 (-0.24, 0.33) 0.22
The sequential modeling approach for the stone marten produced three models with
∆AICc< 2 (Table 5.4.). According to the model averaging the proportion of scrubland,
rabbit availability and fox control intensity explained stone marten occupancy (Table
5.5.). The proportion of scrubland was the most informative covariate and was
positively associated with stone marten occupancy (Table 5.5.; Figure 5.4.). Stone
marten occupancy was negatively related to rabbit availability and positively to red fox
control intensity (Table 5.5.; Figure 5.3.). Stone marten detection probability was
positively related to the proportion of scrubland, although with low weight of evidence
(w= 0.22) (Tables 5.4., 5.5.).
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Figure 5.2. (a) Relationship between occupancy probability (Ψ) of red fox and riparian, dehesa
and scrubland habitat proportions. (b) Relationship between red fox detection probability (p)
(solid line) and red fox control intensity (fox·year-1·km-2). Dashed lines represent the 95% CI
estimated for detection probability.
119
Figure 5.3. Relationship between occupancy probability (Ψ) of red fox (grey lines) and stone marten (black lines) and red fox control intensity (fox·year-1·km-2). Dashed lines represent the 95% CI estimated for occupancy probability of each species.
Figure 5.4. Relationship between occupancy probability (Ψ) of stone marten (solid line) and scrubland habitat proportion. Dashed lines represent the 95% CI estimated for occupancy probability.
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Discussion
The intensity of red fox control was related differently to both site occupancy and
detection probability of red fox and stone marten. On the one hand, the intensity of fox
control was not related to site occupancy of red fox, but it was negatively associated
with red fox detectability. On the other hand, the intensity of red fox control was
positively related to the stone marten occupancy probability but it was not associated
with its detectability. Overall, habitat composition and prey availability were more
important than red fox control to define site occupancy probability of both species.
According to our results, the intensity of fox control was not related to the site
occupancy of red fox. Although differences in occupancy probability have been
interpreted as reflecting differences in abundance, it has been also suggested that
occupancy and abundance address distinctly different aspects of population dynamics
(MacKenzie and Nichols 2004; Mackenzy et al. 2006). Thus, some changes in
population abundance may not be identified using occupancy estimates, and some
changes in site occupancy may not reflect changes in abundance (Towerton et al. 2011).
For example, if foxes use larger areas, then they may spend less time in any given part
of those areas, thus influencing differently occupancy (increasing) and abundance
(decreasing) (Towerton et al. 2011). When territorial adult foxes are removed from an
area, this area is afterwards reoccupied by subadult foxes, which move through the
landscape in search of available territories (Towerton et al. 2011). In our study area, it is
likely that, after intensive fox control, fox population may be dominated by transient
individuals, which have larger home-rages than territorial (Henry et al. 2005). This may
explain not only the lack of association between fox extraction and red fox site
occupancy, but also the apparent low relationship between the latter and population
abundance; this seems to be related in this case with the spatial distribution of red foxes
populations.
Several authors have suggested that there is a close relationship between species’
abundance and its detectability (e.g. Royle and Nichols 2003; McCarhty et al. 2013). In
this regard, the negative relationship between the detection probability of red foxes and
the intensity of fox control might suggest that this could decrease fox abundance. This is
in disagreement with other studies performed in the Iberian Peninsula that reported
similar (Virgós and Travaini 2005), or even higher abundances of foxes (Beja et al.
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2009) in areas where these were controlled than in areas without control. Nevertheless,
these studies did not take into account the intensity of fox control, which could explain
their contrasting results with respect to our study. It is also noteworthy that changes in
the probability of detection may be the response of foxes to other factors like habitat
type or behavioural responses to human disturbances. Interestingly, in our study area the
intensity of fox control does not seem to be related to the overall activity levels of red
foxes (Chapter 6).
The difficulty to reduce fox populations has been demonstrated in several studies; the
effect of fox control on its abundance is variable and depends on various factors, such as
the control method used or the duration of control (Saunders et al. 2010). In our study,
the method employed in localities with the highest rates of fox extraction was neck-
snaring (Table 1), which is considered an efficient method to remove red foxes in Spain
(see Muñoz-Igualada et al. 2008, 2010). Furthermore, fox control effort was sustained at
least during two years before our study in all localities. On the other hand, cage-
trapping and/or shooting were the methods employed in localities with a low level of
fox control (Table 5.1.), and these are usually ineffective to reduce fox abundance
(Baker and Harris 2006; Saunders et al 2010). This could be also the reason why Beja et
al. (2009) did not observe a lower number of foxes where predator control was
employed, but data on fox control intensity were not considered by these authors.
Red fox can use very different habitats due to its high ecological plasticity (Sillero-
Zubiri et al. 2004; Sarmento et al. 2011). In this study, we found that red fox site
occupancy increased with the proportion of riparian habitat, dehesas and scrubland.
According to previous studies, scrublands and dehesas are determinant habitats in
Mediterranean areas for Iberian carnivores, including the red fox (Mangas et al. 2008).
The high relevance of riparian habitat according to our findings is probably due to the
fact that the field sampling was carried out in hot, dry summer. During this season
riparian habitat can become a key habitat for Iberian carnivores in Mediterranean
ecosystems since they find there food, water and protection against high temperatures
(Virgós 2001; Matos et al. 2009). Red fox site occupancy was also positively associated
with rabbit availability, although this relationship was weaker than those found for
habitat types. This is not surprising as rabbits are likely the most profitable prey for
foxes in the Iberian Peninsula, and their consumption by foxes increases when rabbit
numbers increase (Díaz-Ruiz et al. 2013; Delibes-Mateos et al. 2008b).
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Within communities of Iberian mesocarnivores, red foxes could play a dominant
competitor role over some sympatric species, such as the stone marten (Pereira et al.
2012; Monterroso 2013). In addition, the red fox is one of the carnivore species most
often cited as killers of other mesocarnivores like Martes sp. (Palomares and Caro
1999). In this scenario, red fox extraction may benefit the competitor release of
subordinate sympatric mesocarnivores, such as the stone marten. Our results are in
concordance with this, since red fox extraction increased the occupancy probability of
the stone marten. Similarly, in UK the experimental, selective control of Eurasian
badgers, the dominant predator species, was associated with an increase in the densities
of the red fox, the subordinate one (Macdonald et al. 2004; Trewby et al. 2008).
In our study area localities with more intensive fox extraction used fox snaring, which is
a controversial method in the Iberian Peninsula because it allows the capture of non-
target species (Duarte and Vargas 2001; Barrull et al. 2011). Different levels of non-
selective control of red fox populations could alter the carnivore communities with an
increase in the populations of the target species (i.e. red fox), while the populations of
other non-target species (red fox “competitors”), such as the Eurasian badger, the stone
marten and the pine marten, decrease markedly or even disappear (Casanovas et al.
2012; Lozano et al. 2013; Barrull et al. 2014). Contrarily, our results suggest that fox
control may decrease fox abundance and may benefit the occurrence of a competitor the
stone marten. These differences could be probably due to a mainly selective fox control
in the studied localities or that at least the stone marten was not affected by potential
non-selective fox control. However, it is unclear that non-selective predator control does
not occur in our study area, as it has been reported in other Iberian regions (Beja et al.
2009; López et al. 2014).
Stone marten occupancy was significantly higher in areas with higher proportion of
scrubland. This is in accordance with previous studies, which suggest that stone martens
occupy areas with high vegetation cover and structure complexity, including
Mediterranean scrubland. These habitats provide diverse key feeding resources for stone
martens, such as fruits, small mammals or birds (Barrientos and Virgós 2006; Virgós et
al. 2010; Sarmento et al. 2011; Monterroso 2013) as well as refuge areas (Mangas et al.
2008). Stone martens present a generalist feeding behavior mainly based on the
consumption of fruits and small mammals, although rabbits also may represent key
resources for them during spring and summer seasons (Barrientos and Virgós 2006),
123
when our study was conducted. Surprisingly rabbit availability was negatively related to
stone marten site occupancy. This might be an indirect effect of habitat since stone
martens usually avoid landscapes dominated by open areas (Prigioni et al. 2008; Dudús
et al. 2014), where rabbits tend to be more abundant (Virgos et al. 2003; Calvete et al.
2004). In fact, we found lower rabbit availability in sites dominated by closed habitats
like scrublands, riparian areas and forests (authors, unpublished results).
In conclusion, our work shows how the combined use of camera-trapping and
occupancy models provide a useful tool to evaluate the relationship between
management actions and changes in populations of managed species, especially for
species that are difficult to monitor like carnivores. Nevertheless, some relationships
and assumptions of the outcome of occupancy models are not entirely clear, such as the
link between detection probability and population abundance, discussed here. From this
perspective, rigorous experimental studies based on the combination of this new
methodology and good quality abundance data of predators is essential to improve the
knowledge on the effect of predator control on the population dynamics of target and
non-target predators.
Acknowledgements We are very grateful to land owners, game managers, game keepers and hunters who
allowed us to work in their hunting estates, and to the staff of Cabañeros National Park
and Ruidera Natural Park. Special thanks to people who assisted us during the
fieldwork. This study was funded by project ref: CGL2009-10741, by the Spanish
Ministry of Science and Innovation and EU-FEDER funds, EU 7th framework
HUNTing for Sustainability project (212160, FP7-ENV-2007-1), and the project OAPN
352/2011 from the Spanish Organismo Autónomo Parques Nacionales. J. Caro had a
postdoctoral contract financed by the European Social Fund (ESF) and the Junta de
Comunidades de Castilla-La Mancha (Operational Programme FSE 20072013), and M.
Delibes-Mateos a JAE-doc contract funded by CSIC and the ESF. P. Monterroso
provided helpful support with the statistical analyses.
Ethical standards This work was performed in compliance with current Spanish legislation, and follows
the European Union’s recommendations regarding animal welfare. All procedures were
carried out with appropriate permits by the concerned institutions.
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CAPÍTULO 6: Drivers of red fox (Vulpes vulpes) daily activity: prey availability, human disturbance or habitat structure?
Este capítulo ha sido enviado a una revista SCI:
Díaz-Ruiz F, Caro J, Delibes-Mateos M, Arroyo B, Ferreras P (enviado) Drivers of red fox (Vulpes vulpes) daily activity: prey availability, human disturbance or habitat structure?
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Abstract Daily activity patterns in mammals depend on food availability, reproductive stage,
habitat selection, intraspecific interactions and predation risk, among other factors.
Some mammals exhibit behavioral plasticity in activity patterns, which allows them to
adapt to environmental changes. A good example of this can be found in the red fox
(Vulpes vulpes). This species is adapted to living in highly humanized environments,
where it is often culled because it may affect human interests (e.g. through the
consumption of game species or livestock). We assessed the potential main drivers of
the daily activity patterns of the red fox in 12 Iberian Mediterranean areas through the
use of camera traps. Among these, we considered main prey availability, degree of
human disturbance (e.g. distance to human settlements, and intensity of predator
control) and habitat structure. Our results revealed a predominantly crepuscular and
nocturnal activity of foxes with local variations. Although overall daily activity of fox
increased with rabbit availability, the temporal overlap with prey activity was generally
low. In addition, diurnal activity was lower with higher levels of human disturbance (i.e.
closer to human settlements) and increased in dense habitats. Prey availability may
determine red fox daily activity rhythms in areas with low human disturbance. In
contrast, the activity of foxes seems to be determined by other factors like human
presence where human disturbance is higher. Our study shows that in highly adaptable
species daily activity patterns are determined by several interacting drivers, resulting in
complex behavioral patterns.
Key words: camera trap, circadian rhythms, human disturbance, fox control,
Oryctolagus cuniculus.
126
Introduction Daily activity patterns have been defined as adaptive sequences of routines that meet the
time structure of the environment, shaped by evolution and fine-tuned to the actual state
of the environment (Halle 2000). According to this, animals may exhibit behavioral
plasticity in daily activity patterns to decrease mortality risk, balance energy
expenditure and gain, and enhance their fitness (Monterroso et al. 2013). Thus, in
mammals, daily activity is internally regulated by species-specific endogenous clocks
(Kronfeld-Schor and Dayan 2003), but also by ecological factors such as nutritional
requirements (Masi et al. 2009), temporal habitat selection (Chavez and Gese 2006),
intraguild interactions (Di Bitetti et al. 2010) or predation risk (Lima and Dill 1990).
Additionally, mammals, as well as other animals, show behavioral responses to
environmental changes induced by human activities (Tuomainen and Candolin 2011).
Predators are strongly constrained by prey availability, which is defined as the
combination of prey abundance and their accessibility; prey can be abundant but
inaccessible to predators when they are not active or are in inaccessible habitats
(Ontiveros et al. 2005). Daily activity patterns in mammalian predators are thus
considered mainly the result of innate activity rhythms and a response to prey activity
(Giller and Sangpradub 1993), showing in some cases a high level of synchrony with
their prey (Foster et al. 2013; Monterroso et al. 2013). Other external factors explaining
daily activity patterns of mammalian predators include habitat structure or human
disturbance. Predators frequently decrease their activity at daytime in open habitats
(Chavez and Gese 2006), where predator control is conducted (Brook et al. 2012) or
where human activities such as hunting or outdoor recreational activities are common
(Belotti et al. 2012; Ordiz et al. 2012).
We chose the red fox (Vulpes vulpes) as a model to study flexibility of mammalian
predator daily activity patterns due to its high ecological plasticity and capacity of
adaptation to environmental changes. The red fox is the most widely distributed
mammalian carnivore of the world and it is found in many different habitats, where it
can be abundant and feeds on a large variety of foods (Sillero-Zubiri et al. 2004; Díaz-
Ruiz et al. 2013). Although the species is a generalist predator, European wild rabbits
(Oryctolagus cunniculus) are the most profitable prey in the central-southern Iberian
Peninsula (Delibes-Mateos et al. 2008a; Díaz-Ruiz et al. 2013) where foxes include
rabbits in their diet according to their abundance (Delibes-Mateos et al. 2008b). Red
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foxes have adapted to living in highly humanized environments, where they take
advantage of human subsidiary resources (Bino et al. 2010). In addition, it is often
persecuted by humans because it preys on game species and livestock (Sillero-Zubiri et
al. 2004).
Daily rhythms of activity are among the least studied aspects of the ecology and biology
of red foxes. Different studies have shown that red foxes are mainly nocturnal-
crepuscular, a pattern that can be explained by ecological factors such as season, habitat
and prey (Blanco 1986; Cavallini and Lovari 1994; Monterroso et al. 2013).
Additionally, red fox activity may also be influenced by human activities such as
livestock husbandry (Villar et al. 2013) or road traffic (Baker et al. 2007).
Notwithstanding, to our knowledge no studies have examined the simultaneous
influence of ecological (e.g. habitat and prey availability) and human-related factors on
red fox activity.
In Spain the red fox is a game species that can also be legally culled outside the hunting
season with a special permit. Direct shooting and live trapping with cage traps and neck
snares are the methods most used for legal culling (Delibes-Mateos et al. 2013; Díaz-
Ruiz and Ferreras 2013). Fox control is a widespread game management tool in Spain,
where between 70-94% of hunting estates perform predator control, mainly targeted to
red fox (Díaz-Ruiz and Ferreras 2013). In areas where predator control is carried out
more intensively foxes are exposed to a higher ‘risk of predation’ by humans resulting
from their capture or death (Reynolds and Tapper 1996). Thus, fox control could be
related to stronger fox behavioral responses to human presence in these areas. In this
sense, it is known that when hunting constitutes an important source of mortality in a
given species, human presence itself may create a ‘landscape of fear’ and thereby
provoke strong behavioral responses, as it happens in brown bears (Ursus arctos)
(Martin et al. 2010; Ordiz et al. 2012).
We evaluated the plasticity of red fox daily activity in environments with varying levels
of prey availability and human disturbance (e.g. fox control and distance to human
settlements) in Mediterranean areas from central Spain. According to previous studies
on mammal predator’s activity we expected that foxes would adapt their activity pattern
to that of their main prey, when this was available, but that this behavioral pattern could
be disrupted in function of factors, such as habitat composition or human disturbance.
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To assess this, we first tested whether the activity patterns of the red fox were related to
the daily activity of its preferred prey (European wild rabbit). Secondly, we tested the
relationships between the daily activity of red foxes and prey availability, human
disturbance and habitat structure simultaneously.
Material and Methods Study area
The study was conducted in 12 localities within central Spain (Figure 6.1.), with
Mediterranean-continental climate characterized by hot and dry summers, cold winters
and most rainfall occurring during autumn-spring months (Rivas-Martínez et al. 2004).
The landscape was heterogeneous and dominated by Mediterranean scrubland (mainly
Cistus spp. in combination with holm oak Quercus ilex forests), mixed with cereal
croplands and permanent crops such as olive groves (Olea europaea) and vineyards
(Vitis vinifera) and natural pastures. Other less abundant habitats included riparian
habitats, ‘dehesas’ (pastureland with savannah-like open tree layer, mainly dominated
by Mediterranean evergreen oaks) and plantations of pine (Pinus spp.), eucalyptus
(Eucalyptus spp.) and poplar (Populus spp.). Villages and scattered dwellings were
interspersed in the landscape. Surface and habitat composition varied among localities
(see Table 6.1. for a detailed description).
Figure 6.1. Situation of the study localities (1-12) in the Iberian Peninsula.
129
Agriculture and livestock were the main economic activities in all localities, which were
also hunting estates, with the exception of two protected areas (numbers 5 and 11 in
Figure 6.1.), where hunting was not allowed. The main small game species were
European wild rabbit (hereafter rabbit), red-legged partridge (Alectoris rufa) and Iberian
hare (Lepus granatensis). Hunting estates were managed to improve small game
populations, mainly by the provision of supplementary food and water, and predator
control. The intensity of fox control varied among hunting estates (Table 6.1., and see
below).
Table 6.1. Description of study localities. The predominant landscape (agriculture or
scrubland) is indicated along with the habitat types present in each area: Oa: open areas, Scr:
scrubland, Wc: woody crops, Rip: riparian, Fo: forest, Dh: dehesa. ‘Red fox control’ refers to
the number of foxes culled per square km and year. ‘Cameras’ indicate the number of camera-
traps used in each locality. ‘Effort’ (survey effort) is expressed as camera-days, or the sum of
days each camera was active in the field in each locality.
Study site (Map ID)
Area (km2) Locality use Landscape
(Habitat types)
Red fox control
(foxes km-2 year-1)
Sampling Year Cameras Effort
1 20 Hunting estate Agricultural (Oa, Scr, Rip, Wc) 0.08 2010 20 620
2 16 Hunting estate Scrubland (Oa, Scr, Rip) 1.98 2010 15 424
3 50 Hunting estate Agricultural (Oa, Scr, Rip, Wc) 0.89 2011 18 493
4 35.8 Hunting estate Agricultural (Oa, Scr, Rip, Wc) 0.43 2011 17 485
5 21.4 Protected area Scrubland (Oa, Scr, Rip, Dh, Fo) 0 2011 19 682
6 15.6 Hunting estate Scrubland (Oa, Scr, Rip, Wc) 1.30 2011 20 645
7 21.4 Hunting estate Agricultural (Oa, Scr, Rip, Dh) 0 2012 20 495
8 20 Hunting estate Agricultural (Oa, Scr, Rip, Wc) 4.00 2012 20 503
9 9 Hunting estate Scrubland (Oa, Scr, Rip, Dh, Fo) 0.10 2012 15 417
10 9 Hunting estate Agricultural (Oa, Scr, Rip) 2.70 2012 14 372
11 26 Protected area Scrubland (Oa, Scr, Rip) 0 2012 20 529
12 16 Hunting estate Scrubland (Oa, Scr, Rip, Dh, Fo) 0.70 2013 18 463
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Camera trap surveys
Camera-trap surveys were carried out between 2010 and 2013 in late spring and
summer (May-September, Table 6.1.), after the red fox breeding season (Blanco 1998)
and when rabbits reach their highest annual numbers in the Iberian Peninsula (Blanco
and Villafuerte 1993). We used two models of infrared-triggered digital cameras: Leaf
River IR5 (LeafRiver OutDoor Products, Taylorsville, Mississippi, USA) and HCO
ScoutGuard (HCO OutDoor Products, Norcross, Georgia, USA). Camera stations were
regularly deployed with an approximate distance of 1.2 km among neighboring
cameras, ensuring independence between them (Monterroso 2013). The number of
camera traps deployed in each study locality varied from 14 to 20, proportionally to
locality surface (range: 9-35.8 Km2; Table 6.1.). Cameras were mounted on trees
approximately 0.5–1.0 m off the ground and set to record time and date when triggered.
Cameras operated 24 h a day for an average period of 28.4±0.4 days (mean±SE). We
programmed cameras with the minimum time delay between consecutive photos to
maximize the number of photos taken per captured individual, and so assure the species
identification of each event.
In order to increase the detection probability of red fox, we set the sensitivity of the
infrared sensor at the highest level, and used Valerian scent and Iberian lynx (Lynx
pardinus) urine as lures. This combination has been described as an effective attractant
for the red fox (Monterroso et al. 2011). Between 3 and 4 ml of each lure were put in
two independent perforated plastic vials secured to a metal rod. Lures were set at 2-3 m
from each camera trap, and were replenished every two weeks, when cameras were
inspected to check the batteries and to replace memory cards. Consecutive images of the
same species within 30 min interval were considered as the same event (unless animals
were clearly different individuals) and those separated by a longer interval as
independent events (Kelly and Holub 2008; Davis et al. 2011; Monterroso et al. 2013;
Delibes-Mateos et al. 2014).
Relationship between fox and rabbit activity patterns
We studied the activity patterns of both red foxes and rabbits (its main prey) to estimate
the probability of both species concurring in a time period. Probability density functions
of activity for both species were estimated non-parametrically for each locality from
their detection records using kernel density estimates (Ridout and Linkie 2009). Density
131
functions were only estimated in species and localities with > 10 records. We also
estimated for each locality the coefficient of overlap Δ1 as suggested by Ridout and
Linkie (2009) and Linkie and Ridout (2011) for small sample sizes. The coefficient of
overlap ranges from 0 (no overlap) to 1 (complete overlap). The precision of this
estimator was obtained through confidence intervals, as percentile intervals from 500
bootstrap samples (Linkie and Ridout 2011). These analyses were performed in R 3.0.1
(R Core Development Team 2013), using an adaptation of the scripts developed by
Linkie and Ridout (2011) available at
<http://www.kent.ac.uk/ims/personal/msr/overlap.html>.
Relationship between fox activity, rabbit availability, human disturbance and habitat structure
Records of red fox activity were assigned to one of three time periods (Monterroso et al.
2013): i) twilight (between one hour prior to one hour after sunrise and sunset); ii)
diurnal; and iii) nocturnal periods, taking into account the time of sunset and sunrise in
each study site during the sampling period.
A rabbit availability index was calculated as the number of independent detections of
rabbits per 100 trap days in each camera station (Monterroso 2013).
Distance to human settlement has been frequently used as a proxy of human disturbance
(Ordeñana et al. 2010; Ohashi et al. 2013). We calculated the distance (in kilometers) to
the nearest human settlement from each camera using a Geographic Information System
(QGIS 1.8.0; QGIS Development Team 2013).
Fox control data were gathered through face-to-face interviews with game managers of
each hunting estate, conducted before field sampling (at the end of the regular hunting
season, in February). We asked managers about the number of foxes removed in the
previous hunting season (Table 6.1.). We estimated intensity of fox control as the
number of foxes removed per km2 and year (fox·year-1·km-2), and used it as another
index of human disturbance.
Activity patterns could vary between areas dominated by habitats with high vegetation
cover (i.e. shelter for foxes) and those occupied by open habitats (i.e. without shelter).
Hence, we grouped habitat types in two main categories: dense habitats (including
scrubland, forests and riparian habitats) and open habitats (including ‘dehesas’, pasture
132
and crops). Habitat types surrounding each camera trap were identified from CORINE
land-cover 2006 and updated satellite orthophotos (Instituto Geográfico Nacional,
<http://www.ign.es/>) and checked during field works. Using QGIS 1.8.0, we calculated
the percentage of each habitat type (i.e. open versus dense) within a buffer of 200 m
radius around each camera trap (Ordeñana et al. 2010; Monterroso 2013). Either open or
dense habitat was assigned to each camera-trap according to the prevailing category
(>50%) within the buffer.
Generalized Linear Mixed Models (GLMM) were employed to assess red fox activity as
a function of time period (day, twilight and night), rabbit availability, human
disturbance (fox control intensity and distance to human settlement) and habitat type.
The response variable was the number of independent red fox detections for each
camera in a given time period, fitted to a Poisson distribution and a log link function
was used. We calculated the trapping effort in each camera for each period and locality
as follows: trapping effort = nº camera-days × period duration in hours. Trapping effort
was included as an offset in models. Camera trap identity was included as a random
effect nested within study locality, to account for the non-independence of observations
according to these factors. Fixed explanatory effects included: time period and habitat
as categorical variables; distance to human settlement, intensity of fox control and
rabbit availability as continuous variables; and all two-way interactions between time
period and other variables. Analyses were carried out with R 3.0.1 with lme4 package
(Bates and Maechler 2010; R Core Development Team 2013). We performed all
possible combinations of these independent effects, as all of those models were
biologically plausible. For this purpose we used the function dredge (library MuMIn;
Bartoń 2012), selected the models with delta ΔAICc<2, and if no single model
accounted for >90 % of the total model weights we calculated model-averaged
parameter estimates for the variables included in those models (Burnham and Anderson
2002). We assessed whether models were affected by overdispersion, accepting
dispersion parameter levels between 0.5 and 1.5 (Zuur et al. 2009). We checked for
potential collinearity and redundancy of the explanatory variables by analysing the
Variable Inflation Factor (VIF), eliminating variables with VIF values greater than 10
(Belsley et al. 1980).
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Results During a total effort of 6128 trap-days (mean±SE: 511±27 trapping days·locality-1;
Table 1) (all means are presented±SE), we obtained 610 independent detections of red
foxes (51±14 detections·locality-1) and 1190 of rabbits (99±37 detections·locality-1;
Table 6.2.).
Table 6.2. Number of independent detections of red fox and rabbit and coefficient of overlap
(Δ1) of daily activity patterns of red fox and rabbit in each locality. CI95% is the 95% bootstrap
confidence interval.
Study site (Map ID)
Nº Red fox detections
Nº Rabbit detections ∆1 CI 95%
1 17 48 0.48 (0.33-0.67) 2 4 101 - - 3 35 343 0.33 (0.31-0.52) 4 77 176 0.43 (0.36-0.56) 5 38 108 0.60 (0.39-0.66) 6 22 18 0.49 (0.36-0.72) 7 17 0 - - 8 39 12 0.46 (0.29-0.63) 9 89 0 - -
10 48 357 0.26 (0.15-0.32) 11 180 16 0.24 (0.25-0.49) 12 44 11 0.35 (0.11-0.56)
Red fox activity patterns and overlap with rabbit activity
Red foxes were detected in all the studied localities (Table 6.2.). Fox activity density
functions slightly varied among localities, but in general, two major activity peaks
occurred, one after sunset and another before sunrise (Figure 6.2a.). A preliminary test
showed significant differences among the three defined time periods (Kruskal-Wallis
test, H=25.73, p<0.001): activity was most intense during twilight, followed by night-
time and day-time (mean±SE: 1.02 ± 0.22, 0.79±0.11 and 0.17±0.03 detections·100
trapping-hours-1, respectively). This is in agreement with the results obtained in the
second more complex approach using GLMMs (see below).
Rabbits were detected in most localities (Table 6.2.). Rabbit activity density functions
were similar in all localities, revealing a strong bimodal pattern, with a major activity
peak occurring after sunrise and throughout the morning and a second peak before
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sunset (Figure 6.2b.). Rabbit activity significantly differed among periods (Kruskal-
Wallis test, H=34.88, p<0.001): activity was most intense at day-time, followed by
twilight-time and night-time (mean±SE: 1.47±0.42, 0.98±0.33 and 0.22±0.06
detections·100 trapping-hours-1, respectively).
Figure 6.2. Kernel densities of red fox (a) and rabbit (b) activity in study localities (mean:
solid line; range: dashed lines). Vertical dashed lines represent approximate sunrise and sunset
times.
Coefficients of overlap were estimated in nine localities with enough detection of
rabbits and foxes (Table 6.2.). Coefficient of overlap between red fox and rabbit activity
patterns varied widely among localities, ranging from 0.24 to 0.60 (0.40±0.04; Table
6.2. and Figure 6.3.), and it was not correlated with rabbit availability (Pearson´s
correlation= 0.42, p>0.05).
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Figure 6.2. Kernel densities of red fox (a) and rabbit (b) activity in study localities (mean:
solid line; range: dashed lines). Vertical dashed lines represent approximate sunrise and sunset
times.
Rabbit availability, human disturbance and habitat structure as factors explaining red fox activity patterns
Predictor variables showed VIF values below 10 (VIF values <1.26), and therefore all
variables were included in the analysis. Five of the evaluated models showed ΔAICc <2,
involving a total weight of 0.70 (Table 6.3.). None of these models were affected by
overdispersion (dispersion parameter levels: 0.67-0.69). All these models included all
the fixed variables, except fox control, which was not included in two of the selected
models (Table 6.3.). Interactions between time period and the remaining fixed variables
136
were also included in the selected models (Table 6.3.). The most important variables
explaining fox activity were time period, rabbit availability, distance to human
settlement and habitat type, and the interactions between time period and either rabbit
availability or habitat type (Table 6.4.). Fox control and other interactions between
variables were less important to explain the variability in daily activity of foxes (relative
importance < 0.6; Table 6.4.).
Table 6.4. Model averaged coefficients and standard errors of the variables included in the five
best models explaining the red fox activity (number of independent red fox detections for each
camera in a given period). ‘RI’ is the relative variable importance from model average, ‘Time’
is the time period (day, night or twilight), ‘Distance’ is the distance to human settlement, and
‘Rabbit’ is the availability of rabbits.
Variable Estimate SE z RI P value Intercept -3.576 0.455 7.860 - <0.001 Time: Twilight 0.031 0.264 0.119 1 0.905 Time: Day -1.469 0.347 4.232 1 <0.001 Fox Control -13.1 19.2 0.686 0.46 0.492 Habitat: Dense -0.046 0.253 0.181 1 0.856 Distance 0.159 0.062 2.736 1 0.009 Rabbit 0.004 0.001 3.870 1 <0.001 Twilight*Fox Control 3.923 11.06 0.369 0.20 0.712 Twilight*Dense habitat 0.192 0.237 0.811 1 0.417 Twilight*Distance -0.001 0.043 0.036 0.59 0.971 Twilight*Rabbit 0.001 4·10-04 2.037 1 0.041 Day*Fox Control -22.9 11.5 1.979 0.20 0.047 Day*Dense habitat 0.910 0.223 4.082 1 <0.001 Day*Distance -0.076 0.037 2.043 0.59 0.041 Day*Rabbit -0.002 0.001 2.273 1 0.023
Model-averaged parameter estimates revealed that red fox activity was in general lowest
during day-time, and increased with rabbit availability except during daylight
(Twilight*Rabbit interaction and Day*Rabbit interaction, Table 6.4.; Figure 6.4a.).
Diurnal activity of red foxes increased in dense habitats (Day*Dense habitat interaction,
Table 6.4., Figure 6.4.). Red fox activity increased with increasing distance to human
settlements (Table 6.4.; Figure 6.4b.), although that trend was less marked during day-
time (Day*Distance interaction, Table 6.4.), when overall activity was lower anyway
(Figure 6.4b.). Overall fox activity did not change strongly with fox control, but diurnal
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activity decreased where fox control was more intense (Day*Fox control interaction,
Table 6.4.; Figure 6.4c.).
Figure 6.4. Model-averaged relationships between red fox activity (expressed as
detections·100 trapping-hour-1) and: a) Rabbit availability (rabbits·100 trapping-day-1), b)
Distance to human settlements (km), and c) Fox control (fox·year-1·km-2) during the three
periods of the daily cycle (day, twilight and night) at two different habitat types (dense or open).
For plotting the results, data were back-transformed.
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Discussion Our results indicate that the red fox is mainly crepuscular and nocturnal in our study
areas (Figure 6.2a.). This is in agreement with previous studies (Blanco 1986; Servin et
al. 1991; Cavallini and Lovari 1994) and supports that the red fox is ‘facultative
nocturnal’ (Monterroso 2013). As most canids, the red fox has specific evolutionary
adaptations to the night (sight, hearing, smell, Sillero-Zubiri 2009). However, our
results support that it is not phylogenetically constrained to nocturnality, and we found
differences in the activity patterns associated with the different factors.
During our study period (May-September) rabbits showed a main peak of activity in the
first hours of the day and a slight peak about sunset (Figure 6.2b.), i.e. they were mainly
diurnal, unlike foxes, which were mainly crepuscular and nocturnal (Figure 6.2a.). This
means that the overlap between red fox and rabbit activity was in general low (mean
coefficient of overlap=0.40) compared with that described for other mammalian
predator-prey examples (mean coefficients of overlap>0.60; Foster et al. 2013;
Monterroso et al. 2013). Therefore, our results disagree with the opportunistic hunting
theory, which states that predators adjust their activity in order to reduce the foraging
energy expenditure (Sunquist and Sunquist 1989); i.e. adapting their activity to that of
their main prey species (Foster et al. 2013). Nevertheless, this partial lack of synchrony
between predator and its main prey has been previously reported by Arias-Del Razo et
al. (2011) and Monterroso et al. (2013), who interpreted this as a response of prey to
reduce predation risk.
This low overlap between rabbit and fox activity patterns may suggest that prey is not
the most important factor explaining variations in red fox activity patterns. However,
other results show that it has an important influence on them. For example, our findings
also showed that the overall activity of red foxes was higher where rabbits were more
available, especially during twilight. In that time period, the overlap between rabbit and
fox activity was overall highest, and rabbits might be thus more accessible for foxes.
Accordingly, a greater temporal overlap between fox and rabbit would be expected in
areas with higher availability of rabbits. However, this was not observed in our study, as
there was no relationship between the overlap index and the availability of rabbits.
These results could indicate that red foxes do not need a high synchrony with rabbits
where the latter are abundant, and/or that prey-predator patterns may be altered by
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human disturbance, as it has been also suggested for wolves (Canis lupus) and moose
(Alces alces) in Scandinavia (Eriksen et al. 2009; 2011).
In our study, red fox activity was lower in areas closer to human settlements,
particularly during twilight and night, the time of highest fox activity. Several studies
have shown that human disturbance caused by activities such as agriculture,
stockbreeding and outdoor leisure activities, which frequently take place in our study
areas, affect the activity of mammal predators. For example, Matthews et al. (2006) and
Belloti et al. (2012) demonstrated that tourist activities altered the activity patterns of
black bears (Ursus americanus) in Yosemite National Park (USA) and Eurasian lynxes
(Lynx lynx) in the Czech Republic, respectively. The effect of human disturbance on
predator behavior is especially evident when hunting is an important source of mortality
in a given species. In such case, just human presence may create strong behavioral
responses through fear (Martin et al. 2010), which is in accordance with our results.
Red fox culling by humans has been globally identified as an important cause of
mortality in the red fox (Sillero-Zubiri et al. 2004). From this point of view, an effect of
predator control on the activity pattern of the target species could be expected. For
example, in some areas with intense predator control, canids decrease their activity,
especially during the daylight period (Kitchen et al. 2000; Rasmussen and Macdonald
2011; Brook et al. 2012, but see Monteverde and Piudo 2011). However, in our study
red fox decreased its overall activity and particularly its activity in daytime in areas with
intense fox control (thus with higher direct mortality risk), but the importance of fox
control on fox activity was lower than that of other factors in our study. It is possible
that the effect of human activity would be stronger during the hunting season (Ciuti et
al. 2012; Ohashi et al. 2013) than during our field sampling period but this has not been
tested yet. The lack of a strong behavioral response of foxes to predator control
intensity, together with the high influence of human presence on fox activity, could
indicate that “fear to humans” could be an intrinsic behavior in foxes, accentuated by
the historical persecution of this canid by humans in our study area (Vargas 2002).
The circadian variations in habitat use by hunted species in human-modified landscapes
are possibly a response to human presence (Sunquist 1989; Chavez and Gese 2006;
Martin et al. 2010). Therefore, anti-predator behavior in terms of avoidance of human
disturbance may explain the observed increase in fox diurnal activity in dense habitats
140
(Figure 6.4), which would be safer for the canid. In agreement with this, several studies
have reported that red foxes in rural areas select habitats dominated by dense vegetation
during daytime even with human presence (Cavallini and Lovary 1994; Reynolds and
Tapper 1995; Janko et al. 2012).
Our results show that the red fox presents a high degree of behavioral plasticity
adjusting its daily activity rhythms to different ecological scenarios. In this sense, rabbit
availability seems to drive fox daily activity rhythms in a scenario of low human
disturbance where foxes mainly track rabbits, increasing their diurnal activity. However,
where foxes are close to urbanized areas or culled, human disturbance may determine
the activity of red foxes, which is reduced during daytime. Our findings show how
wildlife adapts to different environmental conditions, including human disturbance,
contributing reliable information about an adaptive species such as the red fox.
Acknowledgements We are very grateful to land owners, game managers, game keepers and hunters who
allowed us to work in their hunting estates, and to the staff of Cabañeros National Park
and Ruidera Natural Park. Special thanks to people who assisted us during the
fieldwork. This study was funded by project ref: CGL2009-10741, by the Spanish
Ministry of Science and Innovation and EU-FEDER funds, EU 7th framework
HUNTing for Sustainability project (212160, FP7-ENV-2007-1), and the project OAPN
352/2011 from the Spanish Organismo Autónomo Parques Nacionales. J. Caro had a
postdoctoral contract financed by the European Social Fund (ESF) and the Junta de
Comunidades de Castilla-La Mancha (Operational Programme FSE 20072013), and M.
Delibes-Mateos a JAE-doc contract funded by CSIC and the ESF.
Ethical standards This work was performed in compliance with current Spanish legislation, and follows
the European Union’s recommendations regarding animal welfare. All procedures were
carried out with appropriate permits, by the concerned institutions.
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DISCUSIÓN GENERAL
Existen numerosos trabajos sobre la temática tratada en esta Tesis Doctoral realizados
en diferentes ecosistemas de todo el mundo. No obstante, un alto porcentaje han sido
desarrollados en sistemas muy simplificados, lo cual hace difícil aplicar sus resultados y
conclusiones a sistemas diversos y de mayor complejidad como los presentes en la
Península Ibérica. En este sentido, los resultados obtenidos en esta Tesis Doctoral
aportan nueva información sobre diferentes aspectos de la ecología y gestión de
depredadores generalistas en ecosistemas complejos, como los ibéricos, en donde el
conocimiento científico es más escaso. La mayor parte de los trabajos de esta Tesis han
sido desarrollados en ambientes Mediterráneos de la Península Ibérica, considerados
entre los de mayor biodiversidad a nivel mundial (Blondel y Aronson 1999), y que
ocupan la mayor parte de la Península Ibérica (Rivas- Martínez 1987; Rivas-Martínez et
al. 2004). Teniendo esto en cuenta, la información aportada en esta Tesis puede ser de
utilidad para mejorar la gestión de dos especies generalistas ampliamente distribuidas y
generalmente abundantes como son el zorro y la urraca.
Ecología trófica del zorro y la urraca
Es fundamental estudiar los hábitos alimentarios de los depredadores para comprender
su ecología, así como para entender el papel que desempeñan en los procesos ecológicos
que ocurren en las comunidades de las que forman parte. Además, los hábitos
alimentarios de los depredadores son la principal causa por la cual gran parte de estos
son perseguidos por el hombre (Woodroffe et al. 2005) y, por lo tanto, conocerlos bien
es de vital importancia para la gestión de estas especies. Tanto el zorro común (Vulpes
vulpes, zorro en adelante) como la urraca (Pica pica) son especies ampliamente
distribuidas y abundantes en gran parte de España, por lo que el estudio de su
alimentación es especialmente relevante para evaluar su posible impacto sobre algunas
presas de interés para la conservación, así como sobre especies cinegéticas de interés
socioeconómico (Herranz 2000; Ruiz-Olmo et al. 2003; Fernandez de Simón 2013).
Aunque puede pensarse que la alimentación de estas dos especies es un aspecto de su
ecología suficientemente conocido, algunas cuestiones no han sido tratadas hasta la
fecha. Los capítulos 1 y 2 de esta Tesis Doctoral aportan nueva información sobre la
ecología trófica de estas especies que puede ser útil para mejorar la gestión de sus
poblaciones.
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Para una mejor comprensión de las estrategias tróficas de los depredadores a nivel de
especie es fundamental su estudio a escala biogeográfica, en la que se tienen en cuenta
un amplio rango de condiciones ambientales derivadas de la distribución de la especie
(Daan y Tinbergen 1997). En las últimas décadas se han llevado a cabo estudios de este
tipo con varias especies de carnívoros de tamaño medio como por ejemplo la gineta
(Genetta genetta) (Virgós et al. 1999), la nutria (Lutra lutra) (Clavero et al. 2003) o el
gato montés (Felis silvestris) (Lozano et al. 2006). Este tipo de estudios han supuesto
una mejora substancial en el conocimiento sobre la ecología trófica de estas especies.
Por ejemplo, han puesto de manifiesto que el gato montés, considerado como un
especialista en micromamíferos en latitudes septentrionales, se alimenta en gran medida
de conejos en latitudes meridionales (Oryctolagus cuniculus). De este modo, gracias a
estos estudios, el gato montés ha sido reconsiderado como un depredador especialista
facultativo, que adapta su alimentación a presas energéticamente más rentables cuando
éstas son abundantes (Lozano et al. 2006).
El zorro ha sido definido como un depredador generalista de amplio espectro trófico,
que utiliza los recursos alimentarios de forma oportunista en función de su
disponibilidad o abundancia (Macdonald y Reynolds 2004). Esta consideración está
apoyada por los resultados obtenidos en numerosos trabajos realizados mayormente a
escala local o regional, mientras que no existe ningún trabajo a escala biogeográfica
similar a los citados anteriormente sobre otros carnívoros. El capítulo 1 de esta Tesis
Doctoral analiza la ecología trófica del zorro a escala biogeográfica en la Península
Ibérica a través de una exhaustiva revisión bibliográfica. Los resultados de este capítulo
demuestran el carácter generalista y oportunista del zorro a esta escala, ya que su
alimentación está relacionada con variables geográficas (latitud, longitud y altitud) y
ambientales (hábitat y estacionalidad), que determinan en gran medida la presencia y
abundancia de sus principales alimentos. Concretamente la dieta del zorro presenta un
marcado patrón latitudinal, alimentándose principalmente de conejos e invertebrados en
el sur de la Península Ibérica, mientras que en el norte su dieta está dominada por
micromamíferos, frutos y semillas. Patrones similares han sido descritos para otros
carnívoros de mediano tamaño como el tejón (Meles meles), el gato montés y la gineta
(Virgós et al 1999; Virgós et al. 2005; Lozano et al. 2006).
El conejo es una especie clave en ecosistemas Mediterráneos de la Península Ibérica y
principal recurso alimentario para un importante número de depredadores ibéricos
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(Delibes-Mateos et al. 2007, 2008a). Los resultados de esta Tesis demuestran la
influencia de los conejos en diferentes aspectos de la ecología del zorro. Por un lado,
son una presa preferida, base de la dieta de los zorros en el centro-sur de la Península
Ibérica (capítulo 1). Por otro lado, la disponibilidad o abundancia de conejos influye
notablemente sobre la ecología espacial del zorro, siendo más probable su presencia en
aquellas zonas donde el lagomorfo es abundante (capítulo 5). Finalmente, desde el
punto de vista comportamental se ha demostrado que la actividad diaria del zorro es
mayor en las zonas donde el lagomorfo presenta una mayor disponibilidad (capítulo 6).
Al igual que otras especies generalistas, el zorro presenta respuestas funcionales
alimentarias como mecanismo adaptativo ante las variaciones de sus recursos tróficos
(Hanski et al. 1991; Panek et al. 2013). En el centro-sur de España se ha observado
cómo el consumo de su principal presa, el conejo, es denso-dependiente, es decir
aumenta con la abundancia del lagomorfo (Delibes-Mateos et al. 2008b; Fernandez de
Simón 2013). Así, cuando el conejo no es abundante el zorro adapta su alimentación
incrementando el consumo de otros recursos secundarios (Ferreras et al. 2011). A escala
biogeográfica los micromamíferos parecen ser uno de los principales recursos
alternativos preferidos por los zorros (capítulo 1). Esto es especialmente interesante
desde un punto de vista de conservación de otras especies presa como las aves, ya que,
cuando hay disponibilidad de micromamíferos, no parecen ser seleccionadas como
principal fuente sustitutoria del conejo. Por el contrario, Ferreras et al. (2011)
comprobaron a escala local, en la Reserva Biológica de Doñana, cómo los zorros
incrementaron significativamente el consumo de aves y carroñas de ungulados como
respuesta a la marcada disminución de las poblaciones de conejo tras la llegada de la
enfermedad hemorrágico vírica (EHVc). A pesar de la acentuada disminución de
conejos en gran parte de España durante las últimas décadas (Delibes-Mateos et al.
2009), las poblaciones de zorro no parecen mostrar descensos significativos en su
abundancia (Sobrino et al 2008; Fernandez de Simón 2013; pero ver Ferreras et al.
2011). Ante este escenario de baja disponibilidad de su presa principal y una abundancia
del cánido relativamente constante, posiblemente haya incrementado la presión de
depredación del zorro sobre otras presas, como por ejemplo algunas aves terrestres que
nidifican en el suelo, para las que el zorro es uno de los principales depredadores (Yanes
y Suárez 1996; Herranz 2000; Ruiz-Olmo et al. 2003). Sin embargo, hasta la fecha este
aspecto no ha sido estudiado de forma específica.
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El patrón de alimentación de la urraca ha sido descrito como el de un generalista que
utiliza de forma oportunista diferentes recursos en función de su disponibilidad
(Birkhead 1991). Los resultados obtenidos en esta Tesis indican que la principal fuente
de variabilidad en la dieta de la urraca es la localización geográfica de sus poblaciones,
mientras que factores intrínsecos como el sexo y la edad no parecen tener tanto peso en
su alimentación (capítulo 2). El patrón de consumo de los distintos grupos tróficos en
cada localidad está probablemente relacionado con su disponibilidad. De esta forma el
consumo de cereal no varió entre las dos localidades estudiadas, donde la disponibilidad
de este tipo de alimento era similar. Sin embargo, las urracas pueden seleccionar ciertos
tipos de alimentos independientemente de su disponibilidad, como por ejemplo algunos
grupos de invertebrados (Martínez et al. 1992; Kryštofková et al. 2011). Estudios
previos han documentado una mayor depredación de nidos artificiales por parte de las
urracas durante la fase de incubación (Suvorov et al. 2012), mientras que durante la fase
de crianza de los pollos el consumo de invertebrados se incrementa significativamente
(Martínez et al. 1992; Ponz et al. 1999). De esta manera, las diferencias observadas
entre localidades en el consumo de aves y artrópodos (capítulo 2) podrían estar
determinadas por la fase del ciclo reproductor en la que se encuentran las urracas.
Además, esta hipótesis podría explicar la diferencia encontrada en la diversidad de la
dieta, que sería menor durante la crianza, debido probablemente al elevado consumo de
artrópodos (capítulo 2).
El papel de la urraca como depredador de pequeños vertebrados, concretamente de aves,
y sus huevos, es un aspecto de su ecología muy discutido. Numerosos trabajos muestran
cómo este córvido consume aves y huevos durante la época de reproducción, aunque
estos representan una proporción muy baja en su dieta (Birkhead 1991). En ese sentido,
los resultados obtenidos en el capítulo 2 muestran cómo las urracas se alimentan
principalmente de semillas de cereal y artrópodos en ambientes agrícolas durante la
reproducción. En esta época los artrópodos son la principal fuente de proteínas para las
urracas (Martínez et al. 1992). Cuando la disponibilidad de éstos es baja, las urracas
utilizan, probablemente de forma secundaria, otras fuentes de proteína animal como
pueden ser las aves o sus huevos, incrementándose bajo estas circunstancias la
probabilidad de depredación (Birkhead 1991; capítulo 2). El uso masivo de pesticidas
en la agricultura actual podría haber incrementado la presión de depredación sobre aves
145
por parte de las urracas, al disminuir la disponibilidad de invertebrados. No obstante,
hacen falta estudios adicionales para corroborar esta hipótesis.
Se encontraron restos de cáscara de huevo y plumas atribuibles a perdiz roja en tan solo
dos mollejas, perteneciendo la mayor parte de restos de aves y huevos a paseriformes
(capítulo 2). A priori los resultados del capítulo 2 pueden ser indicativos de que las
urracas no suponen un problema para la dinámica poblacional de otras aves, tal y como
se ha descrito para las poblaciones de varias especies de paseriformes (Gooch 1991;
Chiron y Julliard 2007). Sin embargo, otros estudios identifican a la urraca como uno de
los principales depredadores de nidos de diferentes aves, incluidos los de perdiz roja
(Groom 1993; Herranz 2000; Roos y Pärt 2004; Ferreras et al. 2010), por lo que es
posible que se subestime el consumo de huevos en los estudios de dieta. Esto hace que
no se pueda descartar que la depredación de nidos por la urraca pueda representar un
riesgo para el éxito reproductor de la perdiz roja en un escenario de alta abundancia de
urracas y bajas densidades de perdiz. En estas condiciones, incluso una pequeña
cantidad de huevos depredados podría representar un gran impacto en el éxito
reproductor de la población de perdiz.
Evaluación y mejora de los métodos de captura para el control de zorros y
urracas Los métodos empleados para el control de depredadores generalistas suscitan
controversia entre diferentes sectores. Por un lado, los conservacionistas consideran que
los métodos hasta ahora utilizados no son selectivos, y que eliminan de forma ilegal
individuos de especies de interés para la conservación (Virgós et al. 2010). Igualmente
algunos autores consideran que los criterios para determinar si los métodos se adecúan o
no a los estándares de captura no cruel no son suficientes ni adecuados (Iossa 2007). Por
otro lado, los cazadores consideran que los métodos permitidos para controlar
depredadores generalistas abundantes son escasos y poco eficaces (Delibes-Mateos et
al. 2013).
La resolución exitosa de este tipo de conflictos se produce cuando el resultado es
aceptable para las distintas partes y ninguna de ellas hace valer sus intereses en
detrimento de los de los demás (Redpath et al. 2013). Bajo esta perspectiva, la
prohibición total del control de depredadores no sería la mejor manera de minimizar los
conflictos entre cazadores, gestores de fauna y conservacionistas en relación a la gestión
146
de los depredadores generalistas. Por lo tanto, parece fundamental trabajar en la mejora
de los métodos de control existentes así como en el desarrollo de nuevos sistemas que
permitan un control selectivo y eficiente de especies generalistas que bajo ciertas
condiciones pueden llegar a ser abundantes, como es el caso del zorro y la urraca. De
hecho, la mejora de los métodos legales para el control de depredadores ha sido incluida
en varias Estrategias de Conservación de algunos depredadores amenazados como el
lince ibérico (Lynx pardinus) o el águila imperial ibérica (Aquila adalberti), como
medida de lucha contra el uso de métodos ilegales y masivos como los cebos
envenenados (Fernández-Olalla 2011), que han repuntado en España en los últimos
años (Martínez-Abraín et al. 2013).
El estudio de diferentes sistemas para el control de zorros y urracas quizás sea el
aspecto sobre el control de depredadores al que mayor esfuerzo se ha dedicado en los
últimos años en España (Díaz-Ruiz y Ferreras 2013). Esto se debe principalmente a la
obligatoriedad del cumplimiento de los estándares establecidos en diferentes tratados
internacionales en cuanto a la eficiencia de captura de las especies objetivo, la
selectividad y los daños relacionados con la captura, necesarios para la homologación
de los métodos y su uso legal. Sin embargo, y hasta la fecha, el esfuerzo dedicado a los
métodos para el control de zorro ha sido muy superior al dedicado a los métodos para
urraca (Díaz-Ruiz y Ferreras 2013). Esto probablemente se deba a que por un lado el
control de dicho carnívoro es más habitual que el control de córvidos y a que por otro
lado los métodos habitualmente empleados para zorro son menos efectivos y selectivos
que los empleados para la urraca, y por tanto suscitan una mayor polémica.
En el caso del zorro, se han evaluado en España dos métodos tradicionales (jaulas-
trampa y lazos) y dos nuevos sistemas de captura desarrollados en Norteamérica
(Belisle y Collarum) (Díaz-Ruiz y Ferreras 2013). Según estos estudios, las jaulas-
trampa son poco eficaces y poco selectivas (Tabla 1). Sin embargo, pocos trabajos han
evaluado diferentes variantes en su uso o modificaciones con vistas a incrementar su
eficiencia de captura y selectividad. Hasta la fecha se ha probado el uso de diferentes
cebos (vivos o muertos) (Herranz 2000; Ferreras et al. 2003, 2007), la combinación de
cebos y atrayentes olorosos (Ferreras et al. 2003, 2007) y la incorporación de una
apertura circular en las puertas de la jaula-trampa para facilitar la salida de especies de
menor tamaño que el zorro (Junta de Andalucía 2010) (Tabla 7.1.).
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En el capítulo 3 de esta Tesis se han analizado de forma conjunta los datos obtenidos en
trabajos realizados en Castilla-La Mancha entre 2003 y 2007. El análisis de estos datos
muestra cómo el uso combinado de cebo vivo con orina de zorro como atrayente
oloroso incrementa la eficiencia de captura de zorros de las jaulas-trampa para esta
especie. También se pudo comprobar un ligero descenso en la tasa de captura de
especies no objetivo al utilizar valeriana como atrayente oloroso. Por lo tanto, el uso
combinado de atrayentes y cebos puede mejorar la eficiencia de captura y selectividad
de las jaulas-trampa. Sin embargo, no se encontró una combinación de cebos y
atrayentes que consiguiera de forma simultanea incrementar la eficiencia de captura y la
selectividad de las jaulas-trampa, y en cualquier caso la selectividad sigue siendo muy
baja (< 25%), aunque hay que ser cautos con estos resultados, debido el pequeño
tamaño de muestra. Los resultados de este capítulo coinciden con los de anteriores
trabajos en desaconsejar la homologación de las jaulas-trampa para su uso como método
de control de zorros en los cotos de caza. En cualquier caso estos resultados podrían
servir para mejorar otros métodos destinados a la captura de zorros.
Estudios previos han demostrado cómo el sistema Collarum (lazo propulsado de cuello)
es eficiente y selectivo para la captura de coyotes (Canis latrans) en Norteamérica
(Shivik et al. 2000, 2005). Los distintos ensayos realizados en España con este sistema
empleando una versión específica para zorros, incluidos los descritos en el capítulo 3,
han obtenido resultados similares en cuanto a su selectividad para capturar cánidos y
una eficiencia aceptable para capturar zorros, que puede mejorarse modificando el
diámetro de cierre del lazo (Tabla 7.1.). Aunque se ha señalado la posibilidad de utilizar
esta trampa en zonas con presencia de especies amenazadas como el lince ibérico
(Muñoz-Igualada et al. 2008), en la actualidad se desconoce el riesgo de captura para
esta especie, así como para otros carnívoros amenazados como el lobo (Canis lupus) o
el oso pardo (Ursus arctos). Se necesitan por tanto pruebas específicas en condiciones
controladas (sin el lazo, con registro en video) en zonas con presencia continuada de las
citadas especies amenazadas, o pruebas previas en cautividad que ayuden a esclarecer si
la trampa es inocua para estas especies.
Se considera que otros métodos como los lazos de acero tradicionales (con y sin tope),
así como sus versiones norteamericanas (lazo “americano” y Wisconsin; ver Herranz
2000 y Muñoz-Igualada 2010 respectivamente) son efectivos para capturar zorros y
muestran una mayor selectividad que las jaulas-trampa, siempre y cuando sean
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instalados de forma correcta (Tabla 7.1.). Sin embargo, es necesario matizar que los
lazos sin tope, están totalmente prohibidos en la actualidad por producir graves lesiones
y sufrimiento innecesario a los animales capturados (Herranz 2000; Duarte et al. 2012).
A pesar de que los lazos con tope son un método muy eficaz para capturar zorros, su
homologación en ciertas comunidades autónomas ha suscitado polémica al no
considerarse lo suficientemente selectivo (Barrull et al. 2011). El sistema de captura
Belisle (lazo de pie) ha sido evaluado en dos trabajos, que indican una buena eficiencia
de captura de zorros y una selectividad mayor que las jaulas-trampa, aunque no se ha
considerado suficiente para poder ser homologado (Tabla 7.1.).
De forma general los lazos con tope, el sistema Belisle y el Collarum para zorro
cumplen con los estándares internacionales de captura no cruel, como demuestra que
más del 80% de los animales capturados en los distintos estudios no presentaron
lesiones graves (Muñoz-Igualada et al. 2008, 2010; Junta de Andalucía 2010). En el
caso de las jaulas-trampa, la mayoría de trabajos realizados en España no han podido
evaluar de forma conveniente los daños relacionados con las capturas de zorros, debido
al bajo número de capturas conseguidas (< 20; Tabla 1). Sin embargo, la mayor parte de
estos trabajos encuentran una baja frecuencia de lesiones graves tanto en zorros como
en especies no objeto de control (Herranz 2000; Muñoz-Igualada et al. 2008; Junta de
Andalucía 2010). Estos resultados coinciden con los descritos para las jaulas trampa
usadas para capturar coyotes en Norteamérica (Way et al. 2002; Way 2012). Los
resultados del capítulo 3 son similares a los obtenidos en trabajos previos para las
jaulas-trampa y el sistema Collarum, con una baja frecuencia de lesiones graves. Sin
embargo, el bajo número de capturas conseguidas con ambos sistemas impidió un
análisis pormenorizado similar al realizado en otros trabajos (Muñoz-Igualada et al.
2008; Junta de Andalucía 2010). En cualquier caso para minimizar los daños es
fundamental la revisión de las trampas al menos una vez cada 24 horas, conclusión en la
que todos los trabajos coinciden.
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Tabla 7.1. Resumen de la información recopilada en los estudios que han evaluado los
sistemas de captura de zorro (JT: jaula-trampa, entre paréntesis el nº de entradas; LT: lazo
tradicional; LA: lazo americano; LW: lazo Wisconsin; Bel.: Belisle; Coll.: Collarum). Los
parámetros utilizados en cada estudio han sido estandarizados en función de la información
recopilada. Esfuerzo: expresado en trampas-noche. Zorros: número de zorros capturados. No
buscadas: número de capturas de especies distintas al zorro. Eficiencia de captura: individuos
capturados/1000 trampas-noche. Selectividad ISO: expresado como el % de zorros capturados
con respecto al total de capturas conseguidas. En negrita aparecen los resultados totales
(TOTAL) para cada sistema de captura además de la media±ES para los parámetros Eficiencia
de captura y Selectividad ISO (*). En la localidad de estudio se indica el número de localidades
(N) donde se han evaluado los diferentes métodos de captura y la Comunidad Autónoma (AN:
Andalucía; CLM: Castilla-La Mancha; CL: Castilla y León) (modificado de Díaz-Ruiz y
Ferreras 2013).
A. JAULAS-TRAMPA
Referencia Modelo Localidad Esfuerzo Capturas Eficiencia de
captura de Zorro
Selectividad
ISO % Zorros No buscadas
Herranz (2000) 1 JT(1) N=1 CLM 2576 1 19 0.39 5 JT(1) N=8 CLM 2596 3 86 1.16 3 JT(2) N=1 CLM 363 1 42 2.75 2
Duarte y Vargas (2001) 3 JT N=1 AN 2160 5 61 2.31 8 Ferreras et al. (2003) 2 JT(1-2) N=1 CLM 927 1 7 1.08 13 Moleón et al.(2003) 2 JT N=1 AN 1558 6 25 3.85 19
Ferreras et al. (2007) 2 JT(1-2)
N=2 CLM 1117 5 22 4.48 19
JT1-2) 736 0 12 0.00 0
Muñoz-Igualada et al. (2008) 3
JT(2)
N=4 CL
515 0 13 0.00 0 JT(2) 540 3 2 5.56 60 JT(2) 140 0 1 0.00 0 JT(2) 127 0 1 0.00 0
Junta de Andalucía (2010) 2 JT(2)
N= 2 AN 409 0 16 0.00 0
JT(2)a 417 1 7 2.40 13 TOTAL 14180 26 314 1.71 ± 0.50* 9.58 ± 4*
B. LAZOS
Herranz (2000) 1 LT/LA(con y
sin tope) N=9 CLM 14 506 27 21 1.86 56
Muñoz-Igualada et al. (2010) 3
LT-alar N= 2CLM 13 610 22 5 1.62 81 LW-alar N= 2CLM 9838 21 8 2.13 72
LW-al paso N= 2CLM 8550 21 9 2.46 70
Junta de Andalucía (2010) 2 LW-al paso
N= 1 AN 5363 8 1 1.49 89
LW-alar 22 292 12 10 0.54 55
Duarte et al. (2012) 3 LT-al paso (sin
tope) N= 1 AN 8568 13 7 1.52 65
TOTAL 32 319 124 61 1.66 ± 0.63* 69.8 ± 26.38*
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C. BELISLE
Muñoz-Igualada et al. (2008) 3 Bel. N=4 CL
538 13 5 24.16 72 574 10 2 17.42 83 406 3 4 7.39 43 317 1 2 3.15 33
Junta de Andalucía (2010) 2 Bel. N= 1 AN 1537 8 3 5.20 73
TOTAL 7372 35 16 11.47 ± 4.01* 60.89 ± 9.64* D. COLLARUM
Ferreras et al. (2007) 2 Coll. N=2 CLM 363 1 1 2.76 50 929 2 0 2.15 100
Muñoz-Igualada et al. (2008) 3 Coll. N=4 CL
535 10 1 18.69 91 562 8 1 14.23 89 359 2 0 5.57 100 297 2 0 6.73 100
Junta de Andalucía (2010) 2 Coll.
N= 2 AN 809 1 0 1.24 100
Coll.a 2057 20 0 9.72 100 TOTAL 5911 46 3 7.64 ± 2.20* 91.22 ± 6.11* 1: Tesis Doctoral; 2: Informe técnico; 3:Artículo científico. a: Modelos modificados
Las jaulas-trampa con reclamo vivo de urraca es uno de los métodos más empleados en
España para el control de las poblaciones de este córvido, y los cazadores españoles lo
consideran como un método eficaz para reducir las poblaciones de estas aves (Delibes-
Mateos et al. 2013). A pesar de ello, antes del trabajo que constituye el capítulo 4 de
esta Tesis Doctoral este método no había sido evaluado teniendo en cuenta los
estándares internacionales anteriormente citados. Dos breves ensayos previos habían
mostrado resultados contradictorios sobre la eficiencia de este sistema para capturar
urracas. Así, Herranz (2000) no consiguió capturar ninguna urraca, mientras que
Martínez de Castilla y Martínez (2004) lo consideran un método muy eficiente; además,
ninguno de los dos trabajos aporta información sobre su selectividad y sobre los daños
derivados de las capturas. En el capítulo 4 se evalúa por primera vez de forma
experimental este método de captura para urracas atendiendo a criterios de eficiencia,
selectividad y captura no cruel establecidos en los tratados internacionales. Los
resultados indican que es un método eficiente y muy selectivo (98%) para la captura de
urracas durante su época de reproducción. Además, se trata de un método de captura no
cruel puesto que ninguno de los animales capturados mostró ninguno de los indicadores
de malestar establecidos en los estándares. Al igual que en el caso de los métodos para
zorros, es imprescindible la revisión de las trampas al menos una vez cada 24 horas.
Hasta la fecha este método ha sido evaluado principalmente en zonas agrícolas.
Solamente existe una breve prueba realizada en una zona mixta de monte mediterráneo
y dehesas agrícolas durante época post-reproductora y con baja densidad de urracas, en
la que se capturaron dos ginetas y ninguna urraca (Ferreras et al. 2007).
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Por lo tanto, se necesitan nuevos estudios en escenarios más heterogéneos, con mayor
diversidad y abundancia de otras especies susceptibles de ser capturadas, que permitan
contrastar los resultados obtenidos en este trabajo.
Efectos del control de depredadores sobre las poblaciones de zorros y
urracas
El principal objetivo del control de depredadores es disminuir el impacto de éstos sobre
algunas especies presa, asumiendo por lo general que la extracción de depredadores
conlleva una disminución efectiva en la abundancia de sus poblaciones. Gran parte de
los trabajos existentes sobre control de depredadores evalúan el efecto sobre las
poblaciones de presas que se pretenden fomentar, prestando menor atención al efecto
sobre las poblaciones de la especie controlada (Smith et al. 2010).
La evaluación experimental de la efectividad de las extracciones de zorros para reducir
sus poblaciones es complicada, debido en parte a la dificultad de realizar estimas fiables
de la abundancia de las poblaciones de los carnívoros (incluido el zorro), que requieren
metodologías costosas y sofisticadas (Heydon et al. 2000; Schauster et al. 2002). El
foto-trampeo es un método de muestreo alternativo que, combinado con el uso de
nuevas y potentes herramientas de análisis estadístico, permite caracterizar el estado de
la poblaciones y detectar los cambios asociados a la gestión en especies poco
abundantes y elusivas, como los mamíferos carnívoros (Sarmento et al. 2011; Towerton
et al. 2011; Cove et al. 2012; Schuette et al. 2013).
Recientemente se ha utilizado el foto-trampeo combinado con modelos de ocupación
(del inglés Occupancy models, Mackenzy et al. 2006) para determinar el efecto de las
campañas de control de zorros sobre sus poblaciones y las de sus potenciales presas en
Australia (Towerton et al. 2011). En dicho trabajo no se encontraron diferencias en la
probabilidad de ocupación espacial de los zorros ni en sus índices de actividad tras las
campañas de control. Los resultados obtenidos en el capítulo 5 son similares a estos, ya
que no se observó ninguna relación entre la intensidad de extracción (control) de zorros
y la probabilidad de ocupación. Igualmente, los resultados obtenidos en esta Tesis
Doctoral han puesto de manifiesto la ausencia de relación entre la intensidad del control
de zorros y la actividad diaria de este carnívoro (capítulo 6), al igual que lo observado
en Australia (Towerton et al. 2011). Sin embargo, en el capítulo 5 se encontró una clara
reducción en la probabilidad de detección de zorros en zonas donde el control era
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intenso, lo que contradice la asunción de Towerton et al. (2011) sobre la asunción de
una probabilidad de detección de zorros similar en periodos pre y post extracción de
zorros. Recientemente se ha sugerido que la probabilidad de detección de una especie
está directamente relacionada con su abundancia (McCarthy et al. 2013). Si esta
relación existiera realmente en el caso de los zorros, los resultados del capítulo 5
indicarían que el control de depredadores, a partir de una cierta intensidad de extracción
y con cierta continuidad temporal, podría disminuir la abundancia local de las
poblaciones de zorro. Sin embargo, tanto los resultados de Towerton et al. (2011) como
los obtenidos en los capítulos 5 y 6 sugieren que las estimas de ocupación y los índices
de actividad posiblemente no sean buenas alternativas para evaluar cambios en las
abundancias de las poblaciones de zorro, ya que probablemente reflejan cambios
espaciales y temporales en el uso de los territorios. A pesar de ello, no se conoce con
exactitud la relación entre la abundancia real de determinadas especies, como en este
caso el zorro, y estos índices (estimas de ocupación, índices de actividad y probabilidad
de detección, estimados a partir de datos de foto-trampeo), lo que motivo frecuente de
discusión entre científicos (Anderson 2003; Royle y Nichols 2003; Mackenzie y
Nichols 2004; McCarthy et al. 2013; Sollman et al. 2013). Se necesitan, por lo tanto,
nuevos estudios basados en estimas fiables de la abundancia real de las poblaciones que
ayuden a probar la validez de estas nuevas metodologías de monitoreo para determinar,
entre otros aspectos, las consecuencias de determinadas medidas de gestión de fauna,
como control de zorros. Dichos estudios contribuirán a la mejora en la toma de
decisiones para la gestión de las poblaciones de las especies hacia las que se dirige la
gestión.
A diferencia de lo descrito previamente para los zorros, la abundancia de ciertas aves
como las urracas puede estimarse de forma más precisa mediante diferentes métodos;
entre otros destacan el conteo de nidos en época reproductora (Stoate y Szuczur 2001,
2005), o el método de muestreo de distancias (del inglés distance sampling) que permite
obtener estimas de densidad absoluta (Newson et al. 2008). A pesar de ello, no existen
muchos trabajos que hayan evaluado el efecto de las extracciones de urracas sobre sus
poblaciones. En general indican que el control durante la época de reproducción es
efectivo para la reducción de la abundancia de sus poblaciones a escala local y regional
(Stoate y Szuczur 2001, 2005; Chiron y Julliard 2007). Igualmente en España, Herranz
(2000) observó que mediante la caza de urracas adultas y la destrucción de sus nidos en
153
un coto cinegético se consiguió una rápida y significativa reducción de la abundancia
del córvido. Los resultados obtenidos en el capítulo 4 muestran que las extracciones
experimentales realizadas con jaulas-trampa pueden reducir a corto plazo y a escala
local la densidad de urracas en lugares donde éstas son abundantes. Sin embargo, la
respuesta de las poblaciones de urracas tras el cese de las extracciones fue diferente en
las dos localidades de estudio. Probablemente estas diferencias se deban a las fechas de
inicio y fin del trampeo, desarrollado durante diferentes fases del ciclo reproductor de la
especie en cada una de las localidades. Se ha descrito que el control a lo largo de todo el
ciclo reproductor consigue una disminución en la población mantenida a lo largo del
tiempo, ya que se extraen parte de los individuos flotantes que rápidamente colonizan
los territorios vacantes (Chiron y Julliard 2007). De esta forma los resultados del
capítulo 4 sugieren que el trampeo desarrollado tan solo desde la puesta (inicio del
trampeo) hasta la incubación (final del trampeo) permite la incorporación de individuos
flotantes que probablemente completen el ciclo reproductor, contribuyendo a la
recuperación de la población. Sin embargo, el trampeo desarrollado en fases más
avanzadas del ciclo reproductor (eclosión-crianza de los pollos) no permitiría completar
de forma exitosa la reproducción a los individuos flotantes incorporados a la población,
manteniéndose la abundancia baja. Recientemente se ha descrito que el control de
urracas intensivo y continuado en el espacio y en el tiempo a escala regional puede
disminuir drásticamente las poblaciones de este córvido, llegando en algunos casos a
existir riesgo de extinción local (Chiron y Julliard 2013). En ningún caso esto debería
ser el objetivo o el resultado de cualquier plan de gestión de un depredador generalista
autóctono, como el zorro o la urraca.
Efectos sobre otras especies no objeto de control
Por lo general se suele asumir o esperar un efecto del control de depredadores sobre las
poblaciones de las especies que son objeto directo de la gestión, es decir, el depredador
que es controlado, así como de la(s) presa(s) que se pretenden recuperar o fomentar
(Saunders et al. 2010; Smith et al. 2010). Sin embargo, el control de depredadores
puede afectar a otras especies que no son contempladas en los planes de gestión, como
por ejemplo otros depredadores (Virgós y Travaini 2005), presas secundarias (Henke y
Bryant 1999) o especies que dependen de la especie controlada para completar su ciclo
reproductor (Martínez 2011).
154
El control de depredadores desarrollado en gran parte de los cotos de caza españoles
podría jugar un papel importante en la composición y estructura de las comunidades de
carnívoros presentes en los mismos. Por ejemplo, se ha sugerido que el control no
selectivo e ilegal puede provocar una disminución de las abundancias de carnívoros y de
la riqueza específica de sus comunidades (Virgós y Travaini 2005; Beja et al. 2009). La
extracción ilegal de especies como la garduña o el tejón podría producir reducciones
significativas en sus poblaciones (Barrull et al. 2014) ya que estas especies presentan
menores tasas reproductivas y menor capacidad de dispersión que el zorro (Casanovas
et al 2012). Igualmente la extracción ilegal de competidores podría beneficiar al zorro
que al ver reducida la competencia podría incrementar su abundancia y expandir sus
poblaciones como se ha mostrado en Reino Unido con la extracción de tejones (Trewby
et al. 2008). Se estaría produciendo, por lo tanto, un efecto contrario al buscado con el
control de sus poblaciones (Lozano et al. 2013). Dentro de las comunidades de
mesocarnívoros ibéricos el zorro podría desempeñar un papel de competidor dominante
sobre algunas especies simpátricas de menor tamaño, como la garduña (Pereira et al.
2012; Monterroso 2013). De hecho, se ha citado que los zorros pueden incluso dar
muerte a individuos del género Martes sp. (Palomares y Caro 1999). Bajo estas
condiciones, la extracción intensiva de zorros podría beneficiar a otros mesocarnívoros
simpátricos subordinados, como la garduña. Los resultados del capítulo 5 están en
concordancia con esto, ya que se observó que la extracción de zorros aumentaba la
probabilidad de ocupación por parte de la garduña. Sin embargo, el papel que
desempeña el zorro dentro de las comunidades de mesocarnívoros ibéricos no está claro,
desconociéndose en gran medida las interacciones ecológicas entre estas especies
(Monterroso et al. 2013). Se necesitan, por lo tanto, nuevos estudios sobre las
interacciones ecológicas intragremiales que ayuden a conocer los posibles efectos de las
medidas de control de zorros sobre la estructura de las comunidades de mesocarnívoros.
En el caso de la urraca se desconoce por completo las consecuencias que el control
intensivo de sus poblaciones pueda tener sobre otras especies. Así, el control podría
perjudicar indirectamente al críalo (Clamator glandarius), un ave parásita de los nidos
de urraca, que depende en gran medida de este córvido para completar su ciclo
reproductor (Martínez 2011), o incluso a otras aves que utilizan los nidos abandonados
de urraca para criar. Igualmente se desconoce el efecto del control sobre especies
potencialmente competidoras de la urraca como podría ser el cernícalo común (Falco
155
tinnunculus) u otros córvidos como el arrendajo (Garrulus glandarius) y el rabilargo
(Cyanopica cyanea) con los que comparte ciertas preferencias ecológicas (Chirón y
Julliard 2007; Alonso 2010; Palomino et al. 2011). En estos casos podría existir un
efecto de “liberación” de competidores como lo anteriormente descrito para algunas
especies de mesocarnívoros. La evaluación de estos aspectos es, por lo tanto,
imprescindible en futuros trabajos que pretendan completar el conocimiento sobre el
control poblacional de este córvido.
Efectos sobre el comportamiento de los depredadores objeto de control
Diferentes trabajos indican que especies habitualmente cazadas pueden modificar sus
patrones de comportamiento espacio-temporal como respuesta al riesgo de muerte que
pueden suponer los humanos, siendo estos cambios más acentuados durante la época
hábil de caza (Ordiz et al. 2012; Ohashi et al. 2013). No obstante, en algunos casos la
simple presencia humana puede provocar igualmente fuertes respuestas
comportamentales en estas especies a través del miedo a ser matados (Martin et al.
2010). Por ejemplo, en algunas zonas con intenso control de depredadores se ha
observado como diferentes cánidos disminuyen su actividad diurna haciéndose más
nocturnos (Kitchen et al 2000; Rasmussen y Macdonald 2011; Brook et al 2012). A
pesar de estos ejemplos, uno de los aspectos menos estudiados sobre el control de
depredadores es como este puede influir sobre el comportamiento de la especie que es
objeto de control. En el caso del zorro, los humanos (y sus actividades) constituyen una
de las principales causas de mortalidad para la especie a escala mundial (Sillero-Zubiri
et al. 2004). Desde este punto de vista, cabría esperar cambios en el patrón de actividad
de esta especie asociados a la intensidad del control de depredadores. Los resultados
obtenidos en el capítulo 6 indican que la actividad del zorro es principalmente nocturna
y crepuscular, y que la actividad diurna se reduce en zonas donde el control de
depredadores es intenso. Los resultados de este capítulo también muestran que la
actividad de los zorros es mayor en zonas con poca presencia humana. Esto sugiere que
el “miedo a los humanos" podría ser un comportamiento intrínseco en el zorro,
relativamente independiente del grado de persecución de estos, derivado de la larga
historia de persecución que este cánido ha experimentado en gran parte de España
(Vargas 2002).
156
Respecto a las urracas, Birkhead (1991) observó un comportamiento más esquivo de las
mismas ante la presencia humana en zonas donde éstas eran habitualmente cazadas.
Probablemente los cambios en el comportamiento de estas dos especies generalistas
derivados de las actividades humanas no suponen una amenaza directa para su
supervivencia y conservación, a diferencia de lo señalado para otras especies como el
oso pardo (Ordiz et al. 2012). Sin embargo, se desconocen las consecuencias directas o
indirectas que estos cambios en la actividad puedan suponer sobre otras especies, así
como en el funcionamiento de los ecosistemas de los que forman parte.
Futuras líneas de investigación
La comprensión de la ecología de depredadores generalistas abundantes es fundamental
para poder establecer medidas de gestión adecuadas que permitan conjugar la
conservación de los ecosistemas con un uso sostenible de los recursos naturales
presentes en estos. Los resultados obtenidos en esta Tesis Doctoral aportan información
de valor sobre esta temática, aunque la información existente sigue siendo escasa y a
menudo poco concluyente. De los resultados de este trabajo destacan algunos aspectos
que deberían estudiarse en mayor detalle en el futuro con vistas a mejorar la gestión de
estas especies. A continuación se proponen algunas líneas futuras de investigación
suscitadas a raíz de esta Tesis Doctoral:
El estudio de la alimentación de los depredadores generalistas, sigue siendo un
aspecto fundamental para mejorar la gestión de estas especies. En el caso del
zorro se hacen necesarios estudios a largo plazo que desvelen, entre otras
cuestiones, el papel de los recursos alimentarios secundarios en la dinámica
poblacional del cánido, y en la de sus principales presas. En el caso de la urraca
son necesarios trabajos que determinen su papel como depredador de huevos y
aves; en este sentido es fundamental combinar estudios experimentales en
cautividad y campo para determinar hasta qué punto el consumo de estos tipos
de alimento es subestimado por las metodologías convencionales (análisis de
contenidos de mollejas o de egagrópilas).
Para ninguna de las dos especies generalistas objeto de estudio en esta Tesis, se
ha podido comprobar si pueden llegar a especializarse en el consumo de algún
tipo de alimento en concreto a nivel específico. En este sentido diferentes
trabajos muestran la importancia de la especialización individual en la
157
explotación de ciertos recursos alimentarios por parte de algunos depredadores
generalistas y cómo esto puede ser determinante en la estructuración y dinámica
de las comunidades de presas (Oro et al. 2005; Prught et al. 2008; Araújo et al
2011; Elbroch y Wittmer 2013). Estudios sobre si existe especialización trófica
en ciertos grupos de presas a nivel de individuo en especies como el zorro y la
urraca pueden aportar información relevante para mejorar la gestión de sus
poblaciones y de algunas de sus presas (especialmente para especies
amenazadas), como se ha mostrado en algunas especies de láridos a través del
control selectivo de individuos (ver Sanz-Aguilar et al. 2009).
Es necesario potenciar la investigación sobre la eficacia de medidas de gestión
alternativas al control letal de depredadores. Para ello se necesitan estudios sobre
la eficacia de estas actuaciones en la reducción del impacto de depredación de
algunos depredadores generalistas. A continuación se presentan ejemplos de
algunas medidas sobre las que sería interesante investigar:
- Papel del acceso a fuentes de alimentación subsidiarias de origen antrópico para
depredadores generalistas (Stone y Trost 1991; Bino et al. 2010), cuya
eliminación o control podría servir para reducir las abundancias de los mismos.
- Recuperación y fomento de depredadores apicales (Prugh et al. 2009). Sería
necesario investigar sobre el papel de depredadores como el lobo y el lince
ibérico en la estructuración de las comunidades tanto de otros depredadores
como en las poblaciones de presas.
- Condicionamiento aversivo por sabor. Sería deseable investigar si este método
provoca una reducción de la tasa de depredación sobre ciertas especies
(Marguire et al. 2009), y si permite mejorar la selectividad de algunos métodos
de captura (Phillips y Whinche 2011).
- Control de la fertilidad mediante anticoncepción y/o esterilización. Recientes
estudios muestran que estas medidas pueden ser eficaces para reducir el impacto
de depredación sobre ciertas presas (coyotes en Norteamérica, Seidler et al.
2014) y pueden ser relativamente eficaces para el control del tamaño poblacional
de las poblaciones de zorro (McLeod y Saunders 2014).
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Aunque el control letal debe ser una medida excepcional, es esperable que su
uso a corto o medio plazo siga siendo habitual tanto en programas de
conservación como de gestión de especies cinegéticas (Redpath et al. 2013), al
menos hasta que se encuentren mediadas alternativas efectivas. Aunque se ha
comprobado que es posible mejorar los sistemas de captura para depredadores
generalistas (Phillips y Whinchell 2011; Short et al. 2012; capítulos 3 y 4), aún
es necesario aclarar un buen número de aspectos. Por ejemplo, en esta Tesis
Doctoral se ha demostrado que se puede aumentar tanto la efectividad como la
selectividad de las cajas-trampa usando combinaciones de cebos y atrayentes y
oloroso. Sin embargo, no se ha podido determinar una combinación de estos que
permita mejorar la efectividad y selectividad de estos dispositivos. Por ello, es
importante seguir investigando en este y otros aspectos que permitan la mejora
de los métodos existentes, así como en el desarrollo de nuevos métodos que
cumplan con los diferentes criterios establecidos para la captura no cruel.
Se ha comprobado como las extracciones de urraca durante la época de
reproducción son eficaces para reducir la abundancia de sus poblaciones a corto
plazo. Las diferentes respuestas de las dos poblaciones de urracas estudiadas tras
el cese del trampeo plantean la hipótesis de que un control desarrollado durante
el ciclo reproductor completo, o al menos durante la fase de crianza de los
pollos, podría reducir la abundancia de forma duradera. Serían necesarios
nuevos trabajos experimentales a largo plazo que evalúen esta hipótesis.
Igualmente, sería necesario evaluar las consecuencias ecológicas del control
sobre otras especies no objetivo vinculadas a la dinámica poblacional de este
córvido, como por ejemplo el críalo europeo.
Los resultados de esta Tesis sugieren que la intensidad del control de zorros
podría disminuir la abundancia de los mismos y a un mismo tiempo
desencadenar procesos ecológicos como la “liberación de competidores”. Son
necesarios estudios experimentales para confirmar estos resultados, e igualmente
desvelar el efecto de esta medida de gestión sobre la diversidad y composición
de las comunidades de carnívoros.
Se necesitan nuevos estudios que permitan esclarecer la relación entre los
parámetros estimados mediante metodologías de occupancy a partir de datos de
159
foto-trampeo, como por ejemplo la probabilidad de ocupación y la
detectabilidad, con la abundancia real de las poblaciones de las especies
estudiadas, ya que este aspecto fundamental es todavía causa de debate en la
comunidad científica.
CONCLUSIONES 1. Las variaciones en los hábitos de alimentación de los zorros ibéricos están
relacionadas con variables geográficas, tipos de hábitat y estacionalidad, que a
su vez determinan la disponibilidad de sus principales alimentos. Por lo tanto, la
flexibilidad trófica de este depredador refleja los patrones biogeográficos de la
distribución y abundancia de sus principales fuentes de alimento. No se encontró
ninguna relación significativa de la diversidad de la dieta con las variables
estudiadas. Estos resultados confirman al zorro como un depredador generalista
y oportunista a una escala biogeográfica mayor de lo que se había descrito hasta
ahora.
2. Aunque no llegan a especializarse en ninguno de sus principales recursos
alimentarios, los zorros en la Península Ibérica consumen conejos como
alimento principal en aquellos lugares donde estos son abundantes, y como
principales presas sustitutorias los micromamíferos, frutos y semillas cuando el
lagomorfo no es abundante.
3. La alimentación de la urraca durante su periodo reproductor en ambientes
agrícolas del centro-sur de la Península Ibérica, se basa principalmente en
artrópodos (mayormente coleópteros) y cereales. Las urracas incluyen en su
dieta huevos y aves con baja frecuencia y en baja proporción, por lo que su
impacto de depredación sobre este tipo de presas no parece importante. No
obstante, se desconocen los posibles sesgos asociados a la metodología de
estudio para la estima del consumo de estos alimentos.
4. Tanto el consumo de los principales grupos alimentarios como la diversidad de
la dieta de la urraca varió entre localidades, sin una influencia clara de factores
intrínsecos como el sexo y la edad. El patrón de alimentación observado
coincide con el de una especie generalista que utiliza los recursos en función de
160
su disponibilidad, aunque se podría explicar también en parte por la fase del
ciclo reproductor.
5. El uso combinado de cebos y atrayentes puede mejorar la eficiencia de captura y
selectividad de las jaulas-trampa para capturar zorros. La combinación cebo
vivo-orina de zorro incrementó de forma significativa la eficiencia para capturar
zorros, mientras que el uso de extracto de valeriana consiguió disminuir
ligeramente la tasa de captura de especies no objeto de control. Sin embargo,
ninguna combinación de cebos y atrayentes de las ensayadas permitió de forma
simultanea incrementar la tasa de capturas de zorros y disminuir la de especies
no buscadas, no alcanzándose en ningún caso los umbrales mínimos de
selectividad establecidos como requisitos para su homologación.
6. El sistema de captura Collarum mostró una mayor selectividad que la obtenida
para las jaulas-trampa y una aceptable eficiencia de captura de zorros, superior a
la de las jaulas-trampa sin atrayentes. Los resultados obtenidos con este sistema
indican que es una alternativa aceptable a métodos tradicionales como las jaulas-
trampa para el control poblacional de zorros en cotos de caza de características
similares a los estudiados.
7. Las jaulas-trampa con reclamo de urraca viva, utilizadas durante la época de
reproducción son un método eficaz y muy selectivo para el control de las
poblaciones de urracas en ambientes agrícolas donde el córvido es abundante.
Estos resultados cumplen los estándares de captura establecidos para poder
utilizar estas trampas como método de control en medios agrícolas; sin embargo
se desconoce su funcionamiento en ambientes más complejos, donde exista una
mayor probabilidad de capturas de especies no buscadas.
8. Los sistemas de captura evaluados en esta Tesis no produjeron lesiones
consideradas como indicadores de malestar a ninguna de las especies objetivo,
tanto zorro como urraca. En cualquier caso es fundamental que en las campañas
de control efectuadas con cualquier sistema de captura, todas las trampas
instaladas sean revisadas al menos una vez cada 24 horas para evitar sufrimiento
innecesario a los animales capturados.
161
9. Las extracciones de urracas consiguieron disminuir a corto plazo las densidades
del córvido en las dos localidades de estudio. Sin embargo, la respuesta de las
poblaciones tras el cese del control fue distinta entre ambas localidades. Se
observó una recuperación de la población tras el cese del control cuando las
extracciones se realizaron en las primeras fases del ciclo reproductor (puesta-
incubación), mientras que cuando se realizaron en fases más avanzadas de la
reproducción (eclosión-crianza de los pollos) la población se estabilizó tras el
cese del control a densidades menores.
10. La probabilidad de ocupación espacial por parte de los zorros no se vio afectada
por la intensidad del control de sus poblaciones, estando determinada
principalmente por el tipo de hábitat predominante. Por el contrario, la
probabilidad de detección de zorros disminuye con el incremento en la
intensidad de su control. Si se confirmase la relación positiva entre
detectabilidad y abundancia sugerida por algunos autores, estos resultados
sugerirían que la intensidad de control podría disminuir la abundancia de zorros.
11. La intensidad del control de zorros estuvo relacionada con el incremento en la
probabilidad de ocupación espacial de la garduña. Estos resultados sugieren que
el control intensivo de zorros puede desencadenar procesos de “liberación de
competidores” debido a la disminución numérica del zorro. Al mismo tiempo,
los resultados aportan nueva información sobre el papel desempeñado por cada
especie en una relación competitiva intragremial. De esta forma el zorro
desempeñaría un papel de competidor dominante y la garduña el de competidor
subordinado.
12. El zorro mostró una actividad principalmente crepuscular y nocturna solapando
parcialmente con la actividad de su principal presa, el conejo. Las variables más
relacionadas con su actividad fueron la disponibilidad de conejos y la presencia
humana, independientemente de la intensidad de control de zorros. La
disponibilidad de conejo parece determinar los ritmos de actividad diaria en
situaciones de baja perturbación humana, en las que los zorros incrementan su
actividad diurna para aumentar el solapamiento con la actividad de los conejos.
Sin embargo, la actividad de los zorros se reduce durante el día cerca de zonas
urbanizadas o donde el zorro es sometido a intenso control, como consecuencia
162
de las perturbaciones humanas. Estos resultados demuestran que el zorro
presenta una elevada plasticidad comportamental que le permite adaptarse de
forma exitosa a diferentes condiciones ambientales, incluyendo la perturbación
humana.
163
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APÉNDICES
198
Appendix 1.1. Studies of the diet of the red fox in Iberia used in this review, with an indication of the latitude (Lat.), longitude (Long.) and altitude (Alt.) where the study took place, year, sample size, duration of the study, predominant habitat, season and type of material. The Map ID (see Fig. 1) is also shown.
Reference Lat. Long. Map ID Year Sample
size Study
duration Habitat Season Material
Amores (1975) 38.17 -5.25 1 1973 121 22 M. Scrub Annual Stomach
Angelo (2000) 37.38 -7.63 2 1999 81 9 - Annual Scat
Angelo (2000) 37.38 -7.63 2 1999 42 3 - Winter Scat
Ballesteros & Degollada (2002) 41.68 2.02 3 1997 140 12 Forest Annual Scat
Barrull and Mate (2007) 41.32 0.97 4 2006 985 21 - Annual Scat
Barrull and Mate (2007) 41.32 0.97 4 2006 354 5,25 - Autumn Scat
Barrull and Mate (2007) 41.32 0.97 4 2006 205 5,25 - Spring Scat
Barrull and Mate (2007) 41.32 0.97 4 2006 241 5,25 - Summer Scat
Barrull and Mate (2007) 41.32 0.97 4 2006 185 5,25 - Winter Scat
Bermejo and Guitián (2000) 42.57 -6.63 5 1990 30 4 - Autumn Scat
Bermejo and Guitián (2000) 42.85 -6.82 6 1990 44 3 - Autumn Scat
Blanco (1986) 40.75 -4 7 1984 97 7 Forest Annual Scat
Blanco (1986) 40.75 -4 7 1984 30 2 Forest Autumn Scat
Blanco (1986) 40.75 -4 7 1984 18 2 Forest Spring Scat
Blanco (1986) 40.75 -4 7 1984 49 3 Forest Summer Scat
Blanco (1988) 40.75 -4 7 1985 414 27 Forest Annual Scat
Blanco (1988) 40.75 -4 7 1985 90 6 Forest Autumn Scat
Blanco (1988) 40.75 -4 7 1985 104 9 Forest Spring Scat
Blanco (1988) 40.75 -4 7 1985 131 6 Forest Summer Scat
Blanco (1988) 40.75 -4 7 1985 92 6 Forest Winter Scat
199
Reference Lat. Long. Map ID Year Sample
size Study
duration Habitat Season Material
Narváez, et al. (2008) 37.92 -5.75 8 2005 138 24 M. Scrub Annual Scat
Braña & Del Campo (1980) 43.1 -5.83 9 1978 68 36 Forest Annual Stomach
Calviño et al. (1984) 42.83 -8.22 10 1978 429 84 - Annual Stomach
Calviño et al. (1984) 42.83 -8.22 10 1978 230 21 - Autumn Stomach
Calviño et al. (1984) 42.83 -8.22 10 1978 24 21 - Spring Stomach
Calviño et al. (1984) 42.83 -8.22 10 1978 49 21 - Summer Stomach
Calviño et al. (1984) 42.83 -8.22 10 1978 158 21 - Winter Stomach
Calzada (2000) 37.15 -6.43 11 1996 1295 35 M. Scrub Annual Scat
Carvalho and Gomes (2004) 41.82 -7.78 12 1999 193 12 M. Scrub Annual Scat
Carvalho (2001) 41.82 -7.78 12 2000 193 12 M. Scrub Annual Scat
Carvalho (2001) 41.82 -7.78 12 2000 38 3 M. Scrub Autumn Scat
Carvalho (2001) 41.82 -7.78 12 2000 44 3 M. Scrub Spring Scat
Carvalho (2001) 41.82 -7.78 12 2000 65 3 M. Scrub Summer Scat
Carvalho (2001) 41.82 -7.78 12 2000 46 3 M. Scrub Winter Scat
Castroviejo et al. (1984) 37.15 -6.43 13 1984 81 12 - Annual Stomach
Castroviejo et al. (1984) 40.42 -3.67 14 1984 103 12 - Annual Stomach
Castroviejo et al. (1984) 39.5 -6.33 15 1984 230 12 - Annual Stomach
Castroviejo et al. (1984) 42.42 -8.63 16 1984 120 12 - Annual Stomach
Castroviejo et al. (1984) 43.42 -7.25 17 1984 75 12 - Annual Stomach
De Carvalho and Alves Alexandre (1994) 41.92 -6.6 18 1993 656 12 Forest Annual Scat
Delibes Mateos et al. (2007) 38.48 -4.5 19 2002 35 3 - Summer Scat
Delibes Mateos et al. (2007) 38.48 -4.5 19 2002 24 3 - Summer Scat
Delibes Mateos et al. (2007) 38.48 -4.5 19 2002 25 3 - Summer Scat
200
Reference Lat. Long. Map ID Year Sample
size Study
duration Habitat Season Material
Delibes Mateos et al. (2007) 38.48 -4.5 19 2002 114 3 - Summer Scat
Delibes Mateos et al. (2007) 38.48 -4.5 19 2002 31 3 - Summer Scat
Dos Santos Correia (1993) 40.3 -7.07 20 1991 241 15 Annual Scat
Esmeriz (2001) 40.58 -7.58 21 1998 207 12 Forest Annual Scat
Esmeriz (2001) 40.58 -7.57 21 1998 176 12 Forest Annual Scat
Esmeriz (2001) 40.58 -7.57 21 1998 26 3 Forest Autumn Scat
Esmeriz (2001) 40.58 -7.57 21 1998 48 3 Forest Autumn Scat
Esmeriz (2001) 40.58 -7.57 21 1998 92 3 Forest Spring Scat
Esmeriz (2001) 40.58 -7.57 21 1998 23 3 Forest Spring Scat
Esmeriz (2001) 40.58 -7.57 21 1998 73 3 Forest Summer Scat
Esmeriz (2001) 40.58 -7.57 21 1998 65 3 Forest Summer Scat
Esmeriz (2001) 40.58 -7.57 21 1998 16 3 Forest Winter Scat
Esmeriz (2001) 40.58 -7.57 21 1998 40 3 Forest Winter Scat
Fedriani (1996) 37.15 -6.43 11 1996 129 24 M. Scrub Annual Scat
Fedriani (1996) 37.15 -6.43 11 1996 164 24 Agr/Dehesa Annual Scat
Fedriani et al. (1999) 37.15 -6.43 11 1993 293 26 M. Scrub Annual Scat
Fedriani et al. (1999) 37.15 -6.43 11 1993 99 M. Scrub Spring Scat
Fedriani et al. (1999) 37.15 -6.43 11 1993 123 M. Scrub Summer Scat
Fernández and Ruiz de Azua (2005) 43 -2.83 22 1997 191 5 Forest Spring Scat
González-Prat (1995)a 41.77 4.45 23 1995 - 3 - Autumn Scat
González-Prat (1995)a 42.5 0.58 24 1995 - 3 - Winter Scat
González-Prat (1995)b 41.3 1.8 25 1995 - 12 M. Scrub Annual Scat
Guitian and Callejo (1983) 42.55 -7.27 26 1978 38 60 Agr/Dehesa Annual Scat
201
Reference Lat. Long. Map ID Year Sample
size Study
duration Habitat Season Material
Herranz et al. (1999) 39.5 -2.83 27 1975 105 12 - Annual Stomach
Dos Santos Marques (2003) 40.53 -3.67 28 2002 70 8 M. Scrub Annual Scat
López (1999) 41.8 1.1 29 1999 661 22 - Annual Scat
López (1999) 41.8 1.1 29 1999 113 6 - Autumn Scat
López (1999) 41.8 1.1 29 1999 248 6 - Spring Scat
López (1999) 41.8 1.1 29 1999 143 6 - Summer Scat
López (1999) 41.8 1.1 29 1999 155 4 - Winter Scat
Martín (2008) 41.3 1.8 25 1999 428 11 Annual Scat
Monterroso et al. (2006) 37.65 -7.63 30 2005 45 12 M. Scrub Annual Scat
Negrões (2000) 42.03 -8.13 31 1998 490 24 Agr/Dehesa Annual Scat
Negrões (2000) 42.03 -8.13 31 1997 90 6 Agr/Dehesa Autumn Scat
Negrões (2000) 42.03 -8.13 31 1998 144 6 Agr/Dehesa Spring Scat
Negrões (2000) 42.03 -8.13 31 1998 151 6 Agr/Dehesa Summer Scat
Negrões (2000) 42.03 -8.13 31 1997 105 6 Agr/Dehesa Winter Scat
Padial et al. (2002) 37.07 -3.55 32 1997 132 12 M. Scrub Annual Scat
Padial et al. (2002) 37.13 -3.38 33 1997 74 12 Forest Annual Scat
Palomares and Ruiz-Martínez (1994) 37.37 -2.83 34 1991 38 1 M. Scrub Spring Scat
Palomares and Ruiz-Martínez (1994) 37.37 -2.83 34 1991 90 1 M. Scrub Spring Scat
Sarmento et al. (1999) 40.3 -7.07 20 1996 306 12 M. Scrub Annual Scat
Sarmento et al. (1999) 40.3 -7.07 20 1996 63 3 M. Scrub Autumn Scat
Sarmento et al. (1999) 40.3 -7.07 20 1996 59 3 M. Scrub Spring Scat
Sarmento et al. (1999) 40.3 -7.07 20 1996 125 3 M. Scrub Summer Scat
Sarmento et al. (1999) 40.3 -7.07 20 1996 59 3 M. Scrub Winter Scat
202
Reference Lat. Long. Map ID Year Sample
size Study
duration Habitat Season Material
Such-Sanz (2003) 38.95 -0.58 35 1998 41 4 Agr/Dehesa Summer Scat
Such-Sanz (2003) 39.07 -0.27 36 1998 40 4 Agr/Dehesa Summer Scat
Urios and Plou (1986) 39.42 -0.83 37 1985 237 24 - Annual Stomach
Vericard (1971) 42.52 -0.75 38 1971 66 12 Forest Annual Stomach
Yanes et al. (1996) 36.83 -2.42 39 1993 69 3 M. Scrub Spring Scat
203
Appendix 1.2. Fox diets as described in the reviewed studies (see Figure 1 and Appendix S1). The information is presented as the frequency of occurrence (FO) of each prey group.We also indicate the values of trophic diversity (Herrera diversityindex, D) recorded for each study
Reference ID Lagomorph Micromammals Birds Reptiles Invertebrates Fruits/seed Carrion/garbage D
Amores (1975) 1 71.1 38.8 29.7 0 60.3 0 6.6 12.5
Angelo (2000) 2 11.59 6.04 4.79 0.25 58.69 16.37 0 12.1
Angelo (2000) 2 29.29 16.16 9.09 0 12.12 30.3 3 8.3
Ballesteros and Degollada (2002) 3 1.3 44 12 2 60 60 0 10.3
Barrull and Mate (2007) 4 1.22 12.69 7.51 1.01 41.83 70.86 11.06 7.4
Barrull and Mate (2007) 4 1.41 12.15 4.24 0.56 29.38 80.51 11.86 7.8
Barrull and Mate (2007) 4 0.49 16.1 11.22 0 58.05 43.41 20 8.3
Barrull and Mate (2007) 4 1.24 8.3 8.3 2.9 57.26 70.54 3.73 7.4
Barrull and Mate (2007) 4 1.62 15.67 8.65 0.54 27.57 83.24 9.19 7.5
Bermejo and Guitián (2000) 5 0 16.6 3.3 0 26.6 100 20 9.5
Bermejo and Guitián (2000) 6 0 70.4 22.7 0 20.4 4.5 9.1 9.9
Blanco (1986) 7 9.3 38.1 0 0 47.4 70.1 26.8 12.5
Blanco (1986) 7 0 23.38 0 0 63.3 70 26.66 10.6
Blanco (1986) 7 17.85 67.85 0 0 60.7 7.15 3.55 9.7
Blanco (1986) 7 8.23 34.3 0 0 85.74 46.97 34.66 8.4
Blanco (1988) 7 22 40.3 11.1 2.2 47.3 33.4 20 5.2
Blanco (1988) 7 13.3 28.9 5.6 0 34.4 61.2 22.2 7.0
Blanco (1988) 7 16.3 51 12.5 6.7 53.8 18.3 18.3 4.9
Blanco (1988) 7 10.7 29.8 13.7 1.5 74.8 54.9 27.5 5.1
Blanco (1988) 7 50 52.2 7.6 0 6.5 4.3 8.7 8.3
Narváez et al. (2008) 8 0.7 44.2 6.5 2.9 82.6 8 5 7.7
204
Reference ID Lagomorph Micromammals Birds Reptiles Invertebrates Fruits/seed Carrion/garbage D
Braña and Del Campo (1980) 9 0 64.7 23.52 5.8 45.6 40 19 8.5
Calviño et al. (1984) 10 5.6 53.4 16.5 0.23 49.9 54.1 71.6 5.7
Calviño et al. (1984) 10 2.6 44.7 18.4 2.6 34.2 78.9 2.6 5.4
Calviño et al. (1984) 10 20.5 59.1 6.8 2.3 31.8 2.3 11.4 6.9
Calviño et al. (1984) 10 27.7 24.6 7.7 13.8 55.4 4.6 3.1 6.1
Calviño et al. (1984) 10 10.9 87 13 0 8.7 15.2 0 6.4
Calzada (2000) 11 73 6 9 0 72 16 16 9.1
Carvalho and Gomes (2004) 12 19.6 65.7 10.8 7.8 27.5 17.7 2.9 5.8
Carvalho (2001) 12 17.1 51.3 10.9 5.7 34.7 21.2 4.1 5.8
Carvalho (2001) 12 2.6 44.7 18.4 2.6 34.2 78.9 2.6 6.4
Carvalho (2001) 12 20.5 59.1 6.8 2.3 31.8 2.3 11.4 6.8
Carvalho (2001) 12 27.7 24.6 7.7 13.8 55.4 4.6 3.1 6.2
Carvalho (2001) 12 10.9 87 13 0 8.7 15.2 0 9.8
Castroviejo et al. (1984) 13 0 29 2.5 1.2 3.7 61 37.3 11.1
Castroviejo et al. (1984) 14 13 47 0 0 21 61 25 12.7
Castroviejo et al. (1984) 15 14 34 12 0 35 42 26.5 8.7
Castroviejo et al. (1984) 16 6 33 0.8 0 53 57 10 10.3
Castroviejo et al. (1984) 17 0 34 0 0 25 54.6 26 16.9
De Carvalho and A. Alexandre (1994) 18 7.93 96.96 86.44 0 0 28.97 15.55 12.5
Delibes Mateos et al. (2007) 19 37.2 31.4 62.9 20 91.4 37.1 11.4 3.2
Delibes Mateos et al. (2007) 19 69.6 30.4 39.1 8.7 95.6 17.4 8.7 4.0
Delibes Mateos et al. (2007) 19 84 40 48 12 88 16 12 3.5
Delibes Mateos et al. (2007) 19 49.1 37.7 51.7 14.9 92.1 23.7 7.9 3.6
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Reference ID Lagomorph Micromammals Birds Reptiles Invertebrates Fruits/seed Carrion/garbage D
Delibes Mateos et al. (2007) 19 19.3 48.4 51.6 16.1 93.5 19.3 16.1 3.6
Dos Santos Correia (1993) 20 11.1 23.4 9.9 3.5 36.2 17.3 9.7 6.3
Esmeriz (2001) 21 29 42 27 0 46 51 0 12.1
Esmeriz (2001) 21 1 56 11 0 81 20 0 14.0
Esmeriz (2001) 21 4 51 37 0 51 67 0 8.6
Esmeriz (2001) 21 0 41 3 0 95 27 0 11.5
Esmeriz (2001) 21 26 48 22 0 45 25 0 8.5
Esmeriz (2001) 21 0 73 21 0 82 3 0 11.4
Esmeriz (2001) 21 28 29 26 0 47 76 0 8.1
Esmeriz (2001) 21 0 40 3 0 90 28 0 11.5
Esmeriz (2001) 21 31 43 38 0 38 50 0 8.0
Esmeriz (2001) 21 2 90 12 0 49 10 0 9.9
Fedriani (1996) 11 55.8 7 7 8.5 83.7 24.8 27.1 4.9
Fedriani (1996) 11 53 6.1 16.5 9.1 93.3 6.7 23.1 5.2
Fedriani et al. (1999) 11 53.6 0 0 0 89.1 14.7 22.5 16.8
Fedriani et al. (1999) 11 55.6 0 0 0 92.9 2 19.2 11.7
Fedriani et al. (1999) 11 65 0 0 0 90.2 13 22.8 10.8
Fernández & Ruiz de Azua (2005) 22 1.1 64.3 17.8 2.1 62.3 37.7 17.2 5.9
González-Prat (1995)a 23 33.33 25.93 55.56 0 14.81 66.67 25.93 5.9
González-Prat (1995)a 24 6.67 20 46.67 0 13.33 46.67 93.34 6.4
González-Prat (1995)b 25 24.8 0 18.55 0 8.25 100 15.3 13.2
Guitian and Callejo (1983) 26 0.64 18.82 1.94 0.43 38.96 38.09 0.21 10.5
Herranz et al. (1999) 27 32.4 34.3 37.1 0 20 80 10.5 8.2
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Reference ID Lagomorph Micromammals Birds Reptiles Invertebrates Fruits/seed Carrion/garbage D
Dos Santos Marques (2003) 28 66 24 17 0 11 30 11 9.0
López (1999) 29 33.13 35.1 3.63 0.45 8.17 21.33 1.51 8.3
López (1999) 29 27.43 32.74 2.65 2.65 12.39 36.28 1.76 7.2
López (1999) 29 37.5 41.53 4.44 0 6.85 9.27 1.2 9.2
López (1999) 29 34.97 36.36 4.9 0 12.59 20.28 0 9.8
López (1999) 29 29.03 25.81 1.94 0 2.58 32.9 1.93 9.6
Martín (2008) 25 8.64 8.4 3.7 0 14.7 35.05 5.14 11.1
Monterroso et al. (2006) 30 52.9 44.7 19.9 0 16.5 30.5 0 12.6
Negrões (2000) 31 17.1 44.1 16.3 0.8 54.1 43.1 16.9 5.4
Negrões (2000) 31 17.8 41.1 12.2 1.1 48.9 63.3 10 5.5
Negrões (2000) 31 22.2 47.9 11.8 2.1 47.2 15.3 25.7 5.3
Negrões (2000) 31 12.6 22.5 15.9 0 78.1 68.9 13.9 6.5
Negrões (2000) 31 16.2 72.4 26.7 0 33.3 26.7 15.2 6.4
Padial et al. (2002) 32 24.2 27.3 6.1 4.6 28 41 28.8 5.2
Padial et al. (2002) 33 0 52.7 4.1 1.4 32.4 42 34.2 9.9
Palomares and Ruiz-Martínez (1994) 34 0.7 58.5 8.1 22.2 54.8 14.1 13.3 6.0
Palomares and Ruiz-Martínez (1994) 34 0 72.2 10 11.1 17.8 0 2.2 10.5
Sarmento et al. (1999) 20 7.5 39.9 11.4 7.5 59.1 41.3 7.5 5.3
Sarmento et al. (1999) 20 9.5 27 7.9 3.2 66.7 57.1 11.1 5.5
Sarmento et al. (1999) 20 1.7 59.3 22 16.9 74.6 11.9 10.2 5.4
Sarmento et al. (1999) 20 6.4 28.8 11.2 4 48.8 56.8 3.2 6.1
Sarmento et al. (1999) 20 13.6 62.7 6.8 10.2 69.5 18.6 10.2 5.1
Such-Sanz (2003) 35 22 34 34 10 61 85 0 5.9
207
Reference ID Lagomorph Micromammals Birds Reptiles Invertebrates Fruits/seed Carrion/garbage D
Such-Sanz (2003) 36 25 82 85 3 72 48 0 5.7
Urios and Plou (1986) 37 9.4 13.4 26.3 0.9 17 48.8 12.3 6.5
Vericard (1971) 38 7.6 39.93 15.1 1.5 15.5 39.69 15.47 6.2
Yanes et al. (1996) 39 97.1 2.9 11.6 1.4 49.2 0 8.7 8.7
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Appendix 2.1. Detailed description of magpie diet composition. The No. of analyzed gizzards (Gizzard), and the minimum No. of items found (Items) for each food group are shown. For each food group, we also present the frequency of occurrence (FO), the relative frequency of occurrence (RF) and the average % volume (VOL). Data is independently presented in terms of overall magpie diet (Total) and in each study area (A1 and A2).
Gizzards Items (n = 1016) FO RF VOL Food type Total (n = 118) A1 (n = 61) A2 (n = 57) Total A1 A2 Total A1 A2 Total A1 A2 Total A1 A2 Coleoptera 98 47 51 195 79 116 83.05 77.05 89.47 20.04 13.53 29.82 29.69 14.18 46.30 Formicidae 29 25 4 165 149 16 24.58 40.98 7.02 16.96 25.51 4.11 5.76 10.07 1.16 Isopoda 8 5 3 9 6 3 6.78 8.20 5.26 0.92 1.03 0.77 1.84 1.84 1.84 Hymenoptera 5 2 3 6 2 4 4.24 3.28 5.26 0.62 0.34 1.03 1.97 1.34 2.63 Dermaptera 5 2 3 6 2 4 4.24 3.28 5.26 0.62 0.34 1.03 0.47 0.25 0.70 Araneida 5 3 2 5 3 2 4.24 4.92 3.51 0.51 0.51 0.51 0.64 1.07 0.19 Diptera 1 0 1 1 0 1 0.85 0.00 1.75 0.10 0.00 0.26 0.21 0.00 0.44 Arthropoda larva 1 1 0 2 2 0 0.85 1.64 0.00 0.21 0.34 0.00 0.17 0.33 0.00 Hemiptera 3 2 1 4 2 2 2.54 3.28 1.75 0.41 0.34 0.51 0.39 0.10 0.70 Arthropoda 111 56 55 393 245 148 94.07 91.80 96.49 40.39 41.95 38.05 41.14 29.16 53.96 Gastropoda 11 10 1 20 19 1 9.32 16.39 1.75 2.06 3.25 0.26 3.07 5.89 0.05 Hordeum sp. 27 19 8 274 212 62 22.88 31.15 14.04 28.16 36.30 15.94 14.05 18.77 9.00 Avena sp. 13 2 11 114 6 108 11.02 3.28 19.30 11.72 1.03 27.76 4.92 1.48 8.61 Triticum sp. 8 7 1 36 21 15 6.78 11.48 1.75 3.70 3.60 3.86 2.92 4.26 1.49 Indet. Seeds 31 13 18 66 27 39 26.27 21.31 31.58 6.78 4.62 10.03 14.20 11.92 16.65 Cereal seed 79 43 36 490 266 224 66.95 70.49 63.16 50.36 45.55 57.58 36.10 36.43 35.75 Fruit 5 5 0 5 5 0 4.24 8.20 0.00 0.51 0.86 0.00 1.55 3.00 0.00 Eggs 6 5 1 6 5 1 5.08 8.20 1.75 0.62 1.03 0.26 2.63 3.61 1.58 Other vegetal 40 27 13 39 26 13 33.90 44.26 22.81 4.01 4.45 3.34 10.75 16.20 4.93 Passeriforme 15 13 2 15 13 2 12.71 21.31 3.51 1.54 2.23 0.51 1.20 2.21 0.12 Galliforme 1 1 0 1 1 0 0.85 1.64 0.00 0.10 0.17 0.00 0.04 0.08 0.00 Birds 20 17 3 22 19 3 16.95 27.87 5.26 2.16 3.08 0.77 3.87 5.90 1.70 Apodemus sylvaticus 2 2 0 2 2 0 1.69 3.28 0.00 0.21 0.34 0.00 0.05 0.10 0.00 Felis sp. 1 1 0 1 1 0 0.85 1.64 0.00 0.10 0.17 0.00 0.01 0.02 0.00 Indet. mammal 1 1 0 1 1 0 0.85 1.64 0.00 0.10 0.17 0.00 0.01 0.02 0.00 Mammals 4 4 0 4 4 0 3.39 6.56 0.00 0.41 0.68 0.00 0.07 0.13 0.00 Reptile 1 1 0 1 1 0 0.85 1.64 0.00 0.10 0.17 0.00 0.21 0.41 0.00 Non-food remains Gastrolith 10 8 2 37 33 4 8.47 6.78 1.69 3.64 3.25 0.39 0.51 0.25 0.79 Plastic 5 3 2 6 3 3 4.24 4.92 3.51 0.62 0.51 0.77 0.13 0.18 0.07
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Appendix 2.2.
210
Appendix 2.3.
211
Appendix 3.1. Description and design of the cage-traps models evaluated. Units of size
descriptions are in cm
Model Size Capture
Entrances Live Bait Chamber Capture system (width x length x height)
A 1020 x 2000 x 1000 1 no guillotine-type door+outrigger B 450 x 950 x 500 1 no guillotine-type door+outrigger C 360 x 1450 x 550 2 lateral guillotine-type door+outrigger D 450 x 1520 x 500 2 lateral guillotine-type door+outrigger E 450 x 2300 x 500 2 central guillotine-type door+outrigger
Model A (CT01 type)
212
Model B (CT01 type)
Model C (CT02 type)
213
Model D (CT02 type)
Model E (CT03 type)
214
Appendix 3.2. Overall results obtained for each bait-attractant combination (A). Overall
results obtained for each trap-type-bait-attractant combination (B). Effort: number of trap-nights
Efficiency: foxes/1000 trap-nights; NTcr: non-targets /1000 trap-nights.
Captures Bait Attractant Effort Fox Non-target Efficiency NTcr Selectivity
Dead
Control 654 1 7 1.53 10.71 13 COLL 40 0 0 0.00 0.00 - FAS 138 0 1 0.00 7.25 0 FU 199 0 2 0.00 10.05 0 VAL 72 0 0 0.00 0.00 -
Alive
Control 434 1 14 2.31 32.30 7 COLL 44 0 0 0.00 0.00 - FAS 39 0 1 0.00 25.64 0 FU 205 3 11 14.63 53.66 21 VAL 243 1 4 4.12 16.46 20
Captures CT Type Bait Attractant Effort Fox Non-target Efficiency NTcr Selectivity
A
Dead
Control 8 0 1 0 125.00 0 COLL nt nt nt nt nt nt FAS nt nt nt nt nt nt FU 23 0 1 0 43.48 0 VAL 8 0 0 0 0 -
Alive
Control 137 1 12 7.30 87.59 8 COLL 21 0 0 0 0 - FAS 16 0 1 0 62.5 0 FU 72 2 11 27.78 152.78 15 VAL 86 0 4 0 46.51 0
B
Dead
Control 303 1 4 3.30 13.20 20 COLL nt nt nt nt nt nt FAS nt nt nt nt nt nt FU 120 0 1 0 8.33 0 VAL 16 0 0 0 0 -
Alive
Control nt nt nt nt nt nt COLL nt nt nt nt nt nt FAS nt nt nt nt nt nt FU nt nt nt nt nt nt VAL nt nt nt nt nt nt
C
Dead
Control 343 0 2 0 5.83 0 COLL 40 0 0 0 0 - FAS 138 0 1 0 7.25 0 FU 56 0 0 0 0 - VAL 48 0 0 0 0 -
Alive
Control 297 0 2 0 6.73 0 COLL 23 0 0 0 0 - FAS 23 0 0 0 0 - FU 133 1 0 7.52 0 100 VAL 157 1 0 6.37 0 100
TOTAL 2068 6 40 2.90 19.34 13
(A)
(B)
215
Appendix 4.1. Trap models employed in the experiments: models 1–3 have four capture chambers (a),
whereas model 4 has two capture chambers (b).
a
b
216
Appendix 5.1. Habitat composition of studied sites (%) and rabbit availability (rabbit
detections per 100 trap days) for each study locality (Map ID). Localities are ordered according
to the increasing intensity of fox control.
217
Appendix 5.2. Carnivores detected during camera trap surveys in each locality (Study site). For each species and locality we show the naïve site occupancy (i.e. proportion of cameras that recorded the presence of the species). We show the overall mean naïve occupancy (mean (SE)). “Detection” is the proportion of localities where each species was present. “1-week positive” is the number of positive 1-week sampling occasions and respective proportion (in brackets) over all sampling occasions for mesocarnivores in each of the study localities.
Study site (Map ID) Red fox Stone marten Common genet Egyptian
mongoose Eurasian badger Least weasel Wildcat
1 0.35 nd nd nd nd 0.10 nd 2 0.20 nd nd nd nd nd 0.07 3 0.56 nd nd nd nd 0.06 nd 4 0.59 nd nd 0.12 nd 0.06 nd 5 0.63 0.32 0.26 nd 0.05 nd nd 6 0.50 0.60 0.25 nd 0.05 nd nd 7 0.40 0.20 0.05 0.05 0.05 nd 0.10 8 0.50 0.40 0.05 0.05 0.10 0.05 nd 9 0.87 0.27 0.20 0.07 0.07 nd nd 10 0.57 nd 0.07 0.21 nd nd nd 11 0.95 0.35 0.10 0.10 0.30 nd 0.10 12 0.67 0.33 nd nd nd 0.06 nd
Detection (%) 100 58 58 50 50 42 25
Mean Naïve Occupancy (SE) 0.57 (0.06) 0.21 (0.06) 0.08 (0.03) 0.05 (0.02) 0.05 (0.02) 0.03 (0.01) 0.02 (0.01)
1-week positive 254 (31.7 %) 65 (8.1 %) 22 (2.7 %) 17 (2.1 %) 12 (1.5 %) 5 (0.6 %) 5 (0.6 %)
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