Tesis Fabian Casas

Gestión agraria y cinegética: efectos sobre la perdiz roja
(Alectoris rufa) y aves esteparias protegidas
Memoria presentada por

Fabián Casas Arenas
Para optar al grado de Doctor
VºBº los Directores
Dr. Javier Viñuela Madera Dr. Francois Robert Mougeot
INSTITUTO DE INVESTIGACIÓN EN RECURSOS CINEGÉTICOS

CSIC-UCLM-JCCM
A mis padres y mi hermana
A José Alberto Nieto Arenas, In Memoriam
Es mejor caminar que parar
y ponerse a temblar ….
(Carlos Goñi, Revólver)
Si lo que vas a decir no es más bello

que un silencio, no lo vayas a decir
que hablé el mundo y callé el hombre,
callé el hombre y vuélvase a callar…
(Manolo García)
Índice
ÍNDICE
ESTRUCTURA DE LA TESIS…………………………………………………...… 1
INTRODUCCIÓN………………………………………………………………...…. 3
1. La pseudoestepa agraria ……………………………………….......……... 5
2. La perdiz roja: Importancia en el ecosistema mediterráneo ……………… 6
3. Importancia socioeconómica de la caza de la perdiz roja………………… 7
4. Situación de las poblaciones de perdiz roja ……..……………………….. 8
5. Medidas de gestión cinegética aplicadas a la mejora de las poblaciones
de perdiz …………………………………………..……............................ 10
5.1. Control de depredadores ………………………………………..... 11
5.2. Bebederos y comederos artificiales …………………………….... 12
5.3. Gestión del hábitat ……………………………………………….. 13
5.4. Sueltas de perdices de granja …………………………………….. 14
6. Gestión agraria y cinegética como herramientas de conservación
en la pseudoestepa agrícola ………………………………………………. 16
Objetivos de la tesis……………………………………………………………... 18
Bibliografía……………………………………………………………………… 21
CAPÍTULO 1: Doble incubación, variación en el tamaño de puesta y éxito de
eclosión en la perdiz roja Alectoris rufa: Nueva información dentro de un peculiar
sistema de reproducción en aves …………………………………………………… 31
Abstract ………………………………………………………………………. 33
Introduction …………………………………………………………………... 34
Material and Methods ………………………………………………………… 37
Results ………………………………………………………………………… 41
Discussion …………………………………………………………………….. 45
Acknowledgements …………………………………………………………… 51
References …………………………………………………………………….. 51
CAPÍTULO 2: Prácticas agrícolas o gestión cinegética: ¿Cuál es la clave para
mejorar el éxito reproductivo de la perdiz roja en las pseudoestepas agrarias? ... 57
Abstract ……………………………………………………………………….. 59
Introduction …………………………………………………………………… 59
Material and Methods ………………………………………………………… 62
Results ………………………………………………………………………… 66
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Fabián Casas Arenas
Discussion ……………………………………………………………………. 70
Acknowledgements …………………………………………………………... 74
References ……………………………………………………………………. 74
Electronic Supplementary Material ………………………………………….. 80
CAPÍTULO 3: Consecuencias fenotípicas y sobre la eficacia biológica de la
introgresión genética en poblaciones silvestres de perdiz roja Alectoris rufa …… 83
Abstract ………………………………………………………………………. 85
Introduction ………………………………………………………………….. 86
Material and Methods ………………………………………………………... 89
Results ………………………………………………………………………... 93
Discussion ……………………………………………………………………. 99
Acknowledgements ………………………………………………………….. 105
References …………………………………………………………………… 105
CAPÍTULO 4: Distribución a escala local de los linajes de malaria aviar entre
poblaciones de una especie hospedadora: ¿Un efecto no deseado e infravalorado de
una extendida práctica de gestión? ……………………………………………….. 111
Abstract …………………………………………………………………….... 113
Introduction ………………………………………………………………….. 113
Material and Methods ……………………………………………………….. 116
Results ……………………………………………………………………….. 120
Discussion …………………………………………………………………… 124
References …………………………………………………………………… 129
CAPÍTULO 5: Efecto de la actividad cinegética en el comportamiento y la
distribución espacial del avefría europea, chorlito dorado y sisón común, en el
oeste de Francia: Importancia de los refugios de caza en áreas agrícolas ……... 135
Abstract ……………………………………………………………………… 137
Introduction ………………………………………………………………….. 137
Material and Methods ……………………………………………………...... 140
Results ……………………………………………………………………….. 146
Discussion …………………………………………………………………… 151
References ……………………………………..…………………………….. 157
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Índice
SÍNTESIS ………………………………………………………………………….. 163

Síntesis: Perspectivas de investigación futura y aplicaciones de gestión . 165
Parámetros reproductivos: Nuevos resultados …………………………… 165
¿Gestión del hábitat o control de depredadores? ……………………….... 167
Efectos de las sueltas de perdices de granja ……………………………... 169
Importancia de las reservas de caza ……………………………………… 173
EPÍLOGO: Integración de conservación y gestión agrícola y cinegética .. 174
Bibliografía ………………………………………………………………. 176
CONCLUSIONES …………….…………………………………………………… 181
AGRADECIMIENTOS ……………………………………………………………. 185
i
Estructura de la tesis
ESTRUCTURA DE LA TESIS
Esta tesis esta organizada manteniendo la estructura de cualquier texto científico.

Consta de una Introducción, Objetivos, cinco Capítulos que conforman el cuerpo
principal de esta tesis, un apartado de Síntesis general, y por último las Conclusiones.
La Introducción general, comienza con una descripción del hábitat principal
donde se ha desarrollado la toma de datos de esta tesis, pasando por una descripción de
la importancia ecología de la perdiz roja en el contexto mediterráneo, así como de la
importancia socioeconómica de su caza. Seguidamente se expone una revisión del
estado actual de las poblaciones de perdiz roja, de las principales medidas de gestión
cinegética y sus efectos, y como compatibilizar las actividades tradicionales humanas, la
caza y la conservación de la fauna silvestre en la pseudoestepa agrícola. Para finalizar
con un apartado donde se detallan los Objetivos, que se desarrollaran en cada uno de
los cinco capítulos.
Cada uno de los cinco Capítulos sigue la estructura típica de un artículo
científico. Están redactados en inglés, y reproducen el texto integro de manuscritos que
están en diferente estado de publicación (enviados y en revisión o en preparación) en
revistas científicas internacionales. Solo se han añadido pequeñas modificaciones, como
referencias a otros capítulos de la tesis, o explicaciones algo más detalladas de algunos
aspectos. Aunque las revistas a los que han sido enviados presentas formatos diferentes,
en esta tesis doctoral se ha mantenido un mismo formato para todos los capítulos.
Finalmente, en el apartado de Síntesis se revisan y discuten los resultados
obtenidos y sus implicaciones, tratando de dar una visión integradora, así como de
enunciar una serie de perspectivas futuras de trabajo. Por último, se enumeran las
principales Conclusiones de la tesis.
1
INTRODUCCIÓN
Introducción
1. La pseudoestepa agraria
La pseudoestepa agraria (áreas abiertas muy deforestadas principalmente

destinadas al cultivo de cereales de secano) es uno de los paisajes más característicos de
Europa Occidental, llegando a ocupar un alto porcentaje de la superficie del continente
europeo. En España hasta los años 70-80, estos ecosistemas habían permanecido poco
alterados y en un estado estable de conservación, pero la llegada de los modernos
sistemas de gestión agraria y la intensificación agrícola (concentraciones parcelarias,
homogeneización del paisaje, desaparición de lindes, aumento del regadío, incremento
del uso de agroquímicos, etc.), junto con el abandono de cultivos durante el último
siglo, han modificado la calidad y extensión de hábitat disponible (Chamberlain et al.
2000; Donald et al. 2001; Benton et al. 2003; Brotons et al. 2004; Bota et al. 2005), lo
que es de vital importancia para la conservación de la biodiversidad europea (Pain &
Pienkowski 1997). Esto ha atraído una mayor atención hacia el estudio de los efectos
globales de la gestión agraria en la conservación de la biodiversidad (Tilman et al.
2001; Bota et al. 2005).
Las pseudoestepas constituyen en Europa el hábitat principal de un grupo de
aves representativas de los medios abiertos y con escasa vegetación, denominadas
genéricamente aves esteparias (Suárez et al. 1997). Éstas constituyen un conjunto
filogenético muy heterogéneo de especies que, sin embargo, presentan características
morfológicas, fisiológicas y etológicas similares: (1) nidificación en el suelo o cerca; (2)
coloración críptica; (3) propensión a desplazarse caminando; (4) marcada tendencia al
gregarismo; (5) comportamiento influido por el excesivo sol y la escasez de agua,
incluyendo baños de arena; (6) predominio de cantos aéreos durante el cortejo nupcial,
excepto en especies de gran tamaño; y (7) adaptaciones dirigidas a reducir el impacto de
la depredación del nido. Esta convergencia adaptativa entre especies pertenecientes a
grupos taxonómicos tan distintos se debe a que las adaptaciones se han producido en
múltiples ocasiones de forma independiente (De Juana 2005).
La península Ibérica es una de las zonas de Europa Occidental donde las
pseudoestepas cerealistas presentan mayor extensión. Aparentemente, la situación
ibérica en cuanto a la conservación de estos medios es mucho mejor que la del resto de
Europa, lo que a su vez, aumenta el compromiso por su conservación, ya que es de las
áreas que alberga mayores poblaciones de aves esteparias de Europa (Santos & Suárez
5
Fabián Casas Arenas Tesis Doctoral
2005). Además, estas mismas zonas constituyen el principal área de caza de perdiz roja
en el mundo, especie que, aunque no es considerada estrictamente esteparia, es en estos
medios donde alcanza sus mayores densidades (Blanco-Aguiar et al. 2003; Vargas et al.
2006; Blanco-Aguiar 2007).
2. La Perdiz roja: Importancia en el ecosistema mediterráneo
La perdiz roja (Alectoris rufa) es una galliforme de pequeño-mediano tamaño

endémica del suroeste de Europa. Presenta un característico plumaje, en el que destacan
principalmente el bandeado de las plumas del costado, y el babero negro de las plumas
del cuello, además de una llamativa coloración roja en anillo periocular, pico y patas. Su
distribución natural está restringida a la región mediterránea (España, Portugal, Francia,
noroeste de Italia, y las islas italianas de Elba y Córcega). Además, ha sido introducida
en Reino Unido, islas del Atlántico (Azores, Canarias y Madeira), y con poco éxito, en
Estados Unidos, Nueva Zelanda y Europa central (Blanco-Aguiar et al. 2003). Está
presente en un amplio tipo de hábitats, desde el nivel del mar hasta los 2500 metros de
altitud. Se trata de una especie sedentaria que durante la mayor parte del año exhibe un
comportamiento gregario, siendo sólo durante la época de reproducción
(establecimiento de las parejas, puesta e incubación) cuando presenta un
comportamiento más territorial (Cramp & Simmons 1980). Otro aspecto destacable de
su ecología es una alta productividad, con primeras puestas que suelen variar entre 10 y
18 huevos (Cramp & Simmons 1980; Rueda et al. 1993) y que son puestos con un
intervalo de unos 2 días (Cabezas-Diaz & Virgós 2007). El período de incubación dura
unos 23-24 días (Cramp & Simmons 1980).
La perdiz roja, además de una gran importancia como especie de caza menor,
tiene un alto valor ecológico, ya que es, junto al conejo de monte (Oryctolagus
cuniculus), presa clave de la mayoría de los depredadores ibéricos (Calderón 1983),
incluyendo varias especies endémicas y/o amenazadas, como el águila imperial ibérica
(Aquila adalberti) o el lince ibérico (Linx pardinus). Este papel como presa clave, junto
a la aparición de la enfermedad vírica del conejo, ha podido provocar que, en numerosas
regiones de España la presión cinegética se redirigiera hacia la perdiz, incrementando la
sobreexplotación sus poblaciones (Blanco Aguiar et al. 2004; Blanco-Aguiar 2007). Las
perdices no constituyen la especie de presa principal de ningún depredador ibérico, a
pesar de que se tiene constancia científica de su condición de presa, en al menos alguna
6
Introducción
fase de su ciclo de vida (huevo, pollo o adulto) para 23 aves, 16 mamíferos y 3 reptiles
(Yanes et al. 1998; Casas, F., observación personal). No obstante, se desconoce el
sentido de las relaciones entre las tasas de depredación, la densidad de perdices y sus
depredadores. Una relación de denso-dependencia podría deberse al carácter oportunista
de determinados depredadores como el zorro (Delibes-Mateos et al. 2008), o a la
disminución en la densidad y/o detectabilidad del conejo (Ontiveros et al. 2005). En
cualquier caso, no están claros los efectos de la depredación en la dinámica de
poblaciones, y esta información debería ser uno de los factores más determinantes a la
hora de establecer medidas de gestión adecuadas. Ya que, dada su condición de presa
para múltiples depredadores y de recurso cinegético para el hombre, existe un conflicto
de intereses entre cazadores y depredadores, que normalmente suele resolverse a favor
del hombre, siendo el control de depredadores la herramienta de gestión más utilizada
(Arroyo & Beja 2002). El estudio del efecto de la depredación en la dinámica de
poblaciones de la perdiz roja en el más extendido de sus hábitats, podría ayudar a
clarificar hasta qué punto la depredación es importante, como es aclamado por la
comunidad cinegética, siendo por tanto, una pieza crucial de información para comenzar
a solucionar este conflicto entre gestión cinegética y conservación de la biodiversidad
(Valkama et al. 2005).
A todo lo mencionado anteriormente, habría que añadir su condición de especie
endémica de la región mediterránea (Del Hoyo 1994), tratándose de una de las especies
más emblemáticas que pueblan nuestros campos, que a su vez, le confiere una gran
importancia conservacionista.
3. Importancia socioeconómica de la caza de la perdiz roja
En general, la caza es una importante actividad económica que genera

sustanciales beneficios. Es ésta una de las principales opciones alternativas o
complementarias (agricultura, ganadería,…), para el uso de la tierra de muchos
propietarios en varios países europeos como Reino Unido, Francia, España o Portugal.
Esta actividad tiene un importante valor socioeconómico especialmente en zonas rurales
menos favorecidas, donde tanto el aprovechamiento cinegético como agrícola son la
principal fuente de ingresos (Bernabeu 2000; Howard & Carroll 2001; Martinez et al.
2002).
7
Concretamente, la caza de la perdiz roja es una de las actividades económicas

más importantes en multitud de áreas rurales de España (APROCA 1998; Lucio 1998;
Bernabeu 2000), contando con un arraigo social y cultural únicos. Su caza es
especialmente importante en regiones como Castilla-La Mancha, Andalucía y
Extremadura (Blanco-Aguiar et al. 2003). En conjunto, la caza menor en España
(principalmente conejo y perdiz) genera un movimiento económico de unos 210
millones de euros al año (Ayala 1985). Este montante económico se reparte entre los
arrendatarios de tierras, guardería, ojeadores, licencias, munición, etc., que dan lugar a
que alrededor de la caza exista un importante número de personas que dependen directa
o indirectamente de ella. Adicionalmente, como consecuencia de la gran demanda de
piezas y del declive de las poblaciones silvestres (ver más adelante), otro elemento
importante de la economía existente alrededor de la caza de esta galliforme, y a la vez
de la gestión cinegética, es la suelta de perdices procedentes de granja. En España se
sueltan anualmente entre 3 y 4,5 millones de perdices al año (Garrido 2002). Esto
contribuye al prolífico negocio de la cría de perdices en cautividad, que desde los años
ochenta ha sufrido un incremento sustancial (Blanco-Aguiar 2007). Además, muchas de
estas perdices criadas en granja forman parte de otro floreciente negocio, para consumo
humano, principalmente en la hostelería y en la industria conservera (perdices
escabechadas, patés, etc.).
4. Situación de las poblaciones de perdiz roja
Las poblaciones naturales de perdiz roja han sufrido una marcada regresión en
las últimas décadas en prácticamente toda el área de distribución de la especie (Cramp
& Simmons 1980; Potts 1980; Aebischer & Potts 1994; Aebischer & Lucio 1997), hasta
el punto de ser considerada actualmente especie con estatus de conservación
“vulnerable” a nivel mundial (Aebischer & Potts 1994) y SPEC 2 por BirdLife
Internacional (Tucker & Heath 1994). En España, núcleo central de su distribución y
donde se encuentran las poblaciones más importantes (Aebischer & Potts 1994;
Aebischer & Lucio 1997; Blanco-Aguiar et al. 2003, 2004), su estatus real de
conservación es mal conocido debido a la falta de datos precisos (Blanco-Aguiar et al.
2004).
Diversas razones podrían explicar este declive, pero la más importante parece
ser la alteración del hábitat, particularmente los cambios acontecidos durante las últimas
8
Introducción
décadas en los modelos de gestión agrarios (Lucio & Purroy 1992; Vargas & Cardo
1996; Blanco-Aguiar et al. 2003, 2004; Vargas et al. 2006; Blanco-Aguiar 2007). La
depredación, la sobreexplotación cinegética o problemas asociados a la suelta de
perdices procedentes de granjas (introducción de nuevos patógenos o introgresión
genética), podrían ser también importantes, al menos localmente (Nadal 1992; Millán et
al. 2004; Blanco-Aguiar 2007; Villanúa et al. en prensa). Sin embargo, no está claro
cual es la importancia relativa de este complejo grupo de factores.
Recientemente ha sido realizado el primer análisis a largo plazo de las bolsas de
caza de perdiz roja en España (Blanco-Aguiar 2007). Dicho autor concluyó que la
intensificación agrícola, junto con la sobreexplotación cinegética de las poblaciones en
declive, son los principales factores que explican la disminución en las rentas
cinegéticas de perdiz durante las últimas décadas, sólo recuperadas recientemente
gracias a la generalización de las sueltas. Pero aún conociendo esto, poco se sabe sobre
cuales de los múltiples cambios que la modernización en los sistemas de explotación
agraria ha producido en el ecosistema, están detrás del declive de las poblaciones de
perdiz roja.
Actualmente, las mejores estimas disponibles sobre tendencias poblacionales de
aves comunes en España son las del Programa SACRE de SEO/BirdLife. Los informes
anuales de dicho programa apuntaban una tendencia a la disminución en las poblaciones
de perdiz roja, si bien el más reciente (2007) ya sugiere una estabilidad a largo plazo
con fuertes fluctuaciones interanuales (véanse diferencias en las tendencias poblaciones
entre los informes de 2004 y 2005; SEO/BirdLife 2006, 2007), lo que contrasta con lo
expuesto anteriormente. Por tanto, ¿Qué esta ocurriendo realmente con las poblaciones
naturales de perdiz roja en los últimos años? Parece claro, a tenor de lo acontecido en
buena parte del área de distribución de la especie, que en las últimas décadas ha existido
un declive generalizado de sus poblaciones, concretamente durante la década de los 70
(Blanco-Aguiar 2007), si bien, una posible explicación a esta aparente estabilidad actual
sería que las poblaciones se mantengan constantes, pero a unas densidades inferiores.
No obstante, hay que tener en cuenta que la perdiz roja es una especie eminentemente
mediterránea, y por tanto sometida a una alta variabilidad climatológica interanual y
elevada presión cinegética, factores que afectan directamente a su productividad anual y
mortalidad invernal (Lucio 1990), y por tanto a las densidades en primavera. Así pues,
aunque el programa SACRE desarrollado por SEO/BirdLife aunque ya recoge datos de
9
una cantidad considerable de años (1996-2005), serían necesarias series más largas para
establecer tendencias inequívocas.
Adicionalmente, tanto para mantener poblaciones cazables como para
incrementar el rendimiento económico de las explotaciones cinegéticas, se ha recurrido
a las sueltas de perdices procedentes de granja como herramienta de gestión de uso
común. Paradójicamente, esta liberación masiva de perdices no sólo no ha contribuido a
una recuperación de las poblaciones naturales de perdiz roja, si no que se sospecha que
la introducción de estos ejemplares incluso ha podido agravar la situación de las
poblaciones silvestres (Dowell 1992). Esto hace todavía más complejo desentramar
cuales son los factores que pueden influir en la tendencia poblacional de esta especie.
A todo lo anterior, a pesar de la mencionada importancia tanto ecológica como
socioeconómica de esta especie, habría que añadir que el conocimiento de la biología
general de la perdiz roja en España es relativamente pobre, más si cabe cuando este tipo
de información es clave para el desarrollo de medidas de gestión y planes de
conservación efectivos. Además, resultaba sorprendente encontrar más información
sobre la población de perdiz roja introducida en el Reino Unido (Potts 1980; 1986;
Green 1983; 1984a; 1984b; Rands 1986; 1987a; 1987b; 1988) que sobre la población
autóctona ibérica. Aunque recientemente esta tendencia parece estar invirtiéndose con
una proliferación de nuevos trabajos sobre diversos aspectos de la biología de la perdiz
(Fortuna 2002; Millán 2004; Alonso et al. 2005; Vargas et al. 2006; Pérez-Rodríguez
2007; Blanco-Aguiar 2007; Villanúa 2007; Cabezas-Diaz & Virgos 2007; Tapia &
Domínguez 2007), aún hay aspectos clave de los que se carece de la suficiente
información, sobre todo de aquellos concernientes a la gestión cinegética.
5. Medidas de gestión cinegética aplicadas a la mejora de las poblaciones de perdiz
Dada la recalcada importancia económica, social, ecológica y conservacionista

de la perdiz roja, ésta (al igual que muchas otras especies cinegéticas) puede actuar
como especie “paraguas”, ya que muchas de las acciones encaminadas para mejorar el
rendimiento y conservación de sus poblaciones pueden resultar igualmente beneficiosas
para otras especies que comparten su hábitat. En cambio, unas medidas de gestión
ineficaces o mal establecidas, pueden producir el efecto contrario.
Debido a la mayor importancia socio-económica, las medidas de gestión más
extendidas en los hábitats que ocupa la especie van a ir dirigidas a aumentar el
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Introducción
rendimiento cinegético de sus poblaciones, y son por tanto mucho más generalizadas
que las emprendidas para la gestión de otras especies amenazadas. Este hecho
condiciona de forma importante, sin lugar a dudas, el devenir tanto de las poblaciones
silvestres de perdiz como de las poblaciones de otras especies con las que comparte el
mismo medio. Entre las medidas de gestión cinegética de más amplio uso destacan el
control de depredadores, la colocación de bebederos y comederos, la gestión del hábitat,
y la repoblación con perdices procedentes de granja. Ésta última es sin duda la medida
de gestión que recientemente esta creciendo en adeptos, muy posiblemente por la fuerte
relación positiva entre costes y beneficios a corto plazo (Díaz 2006).
5.1. Control de depredadores
El control de depredadores es una de las herramientas de gestión más extendidas

para fomentar las especies de caza menor (Arroyo & Beja 2002; Díaz 2006), a pesar de
la escasez de información que se tiene sobre el efecto de la depredación en estas
especies (Herranz et al. 2002; Delibes-Mateos et al. en prensa) y, más concretamente,
sobre la dinámica de poblaciones de la perdiz roja.
En cambio, en otras especies cinegéticas como la perdiz pardilla (Perdix perdix),
para la que existe más información, se ha demostrado que el control de depredadores
puede contribuir a un aumento de su éxito reproductivo, incrementando a su vez la
densidad poblacional (Tapper et al. 1996). Por otro lado, otras especies podrían
beneficiarse de una disminución en los tamaños poblacionales de los depredadores,
aumentando su éxito reproductivo, especialmente aquellas más sensibles a la
depredación de nidos por especies generalistas como zorros (Vulpes vulpes) y urracas
(Pica Pica; Yanes & Suárez 1996; De Borbón et al. 1999). Sin embargo, la información
disponible sobre el efecto de esta práctica de gestión en otras especies diferentes a las
cinegéticas es muy escasa (Arroyo & Beja 2002). Sí es conocido, sin embargo, que un
control de depredadores mal realizado puede generar una pérdida de biodiversidad
dentro del gremio de los carnívoros terrestres (Virgós & Travaini 2005), que suelen ser
el grupo sobre el que se suelen centrar los objetivos de control.
Finalmente, la comunidad cinegética a menudo considera la depredación como
el principal factor que existe detrás de la reducción en el éxito reproductor de la perdiz
roja y otras especies cinegéticas de caza menor (Nadal & Comalrena 1994). Esta
percepción, junto con la protección legal de los depredadores y una reducción en la
11
tramitación de los permisos de dichos controles (Nadal 1998), ha supuesto a menudo

una intensificación en el control de depredadores, legal y/o ilegal, que ha afectado
negativamente a las poblaciones de especies amenazadas (Viñuela & Villafuerte 2003).
Esto puede ser debido a que, en la mayoría de los casos los sistemas empleados para la
captura de depredadores generalistas no suelen ser selectivos, como en el caso del uso
de cebos envenenados, que se ha convertido en uno de los mayores problemas de
conservación de especies amenazadas en los últimos años (ADENA 2006). En cuanto al
uso de trampas y otros medios de retención de los depredadores, en el mejor de los
casos, la selectividad y la liberación o no de aquellas especies no contempladas dentro
del objetivo de control, queda sujeta a la ética del personal que revisa las trampas.
5.2. Bebederos y comederos artificiales
Otro de los elementos de gestión más extendidos es la colocación de comederos

(en los que se suele aportar grano) y bebederos artificiales para perdiz. Se ha
demostrado que la abundancia y distribución de puntos de agua pueden determinar los
patrones de distribución y abundancia de la perdiz roja en áreas de estudio portuguesas
(Borralho et al. 1998). Sin embargo, hasta donde sabemos, no parecen ser un elemento
muy usado por las perdices pero sí por otras especies (Casas et al. 2006). No obstante,
los estudios sobre el uso de los bebederos por parte de las aves, incluyendo la propia
perdiz roja, son muy escasos, hasta el punto de que el propio sector cinegético reconoce
que no está nada clara la utilidad o necesidad de estos aportes artificiales (Díaz 2006).
Por otro lado, el aporte suplementario de alimento podría contribuir a una mejora
en la condición física de las aves durante la estación reproductora (Draycott et al. 2002).
En otras especies de aves cinegéticas, esta herramienta de gestión no siempre contribuye
a incrementar el tamaño de puesta o mejorar el éxito reproductivo (Hoodless et al.
1999), aunque puede ayudar a incrementar la densidad de pollos (Draycott et al. 2005).
Para la perdiz roja, el aporte suplementario de alimento es una herramienta de gestión
frecuente (Díaz 2006). No obstante, muy poco se conoce sobre su efecto en los
parámetros reproductivos de la especie. Si la disponibilidad de alimento es un factor
limitante tanto para la reproducción como para la supervivencia, la colocación de
comederos podría ser una medida beneficiosa, pero se precisa de investigaciones
rigurosas para explorar los efectos del alimento suplementario, tanto en la reproducción
como en la supervivencia y condición física de las aves.
12
Introducción
Por otra parte, el suplemento artificial de agua y comida podrían tener incluso
consecuencias negativas para la perdiz roja u otras especies, por constituir comederos y
bebederos puntos de diseminación y transmisión de enfermedades (Vicente et al. 2007),
de atracción de depredadores y furtivos (Díaz 2006), o por alterar la alimentación
suplementaria la anatomía interna, fisiología y comportamiento de las perdices (Millán
et al. 2003).
5.3. Gestión del hábitat
La estrategia de gestión del hábitat llevada a cabo por gestores cinegéticos está
muy condicionada por el tipo de ecosistema y por los aprovechamientos primarios y
secundarios que se obtienen de éste. En función de cual de los aprovechamientos
obtenidos tenga mayor prioridad, las medidas adoptadas beneficiaran en mayor o menor
medida a las poblaciones de perdiz.
En medios pseudoesteparios, las acciones sobre la gestión agraria
(mantenimiento de barbechos y lindes, reducción de laboreo en fechas críticas, cosecha
tardía, etc.) serían la principal estrategia para mejorar la productividad de la perdiz roja,
que a su vez, podrían ser favorables tanto para otras especies cinegéticas como para
otras especies con las que comparte hábitat (Stoate et al. 2004; Parish & Sotherton
2004). Aunque en otros países europeos existen programas establecidos entre cazadores
y agricultores, y los “cultivos cinegéticos” son una de las estrategias de gestión más
utilizadas (Stoate & Szczur 2001; Stoate et al. 2004; Parish & Sotherton 2004; Sage et
al. 2005), en España existen pocos ejemplos, la mayoría reducidos a grandes fincas
donde los cultivos tienen un aprovechamiento secundario.
Desafortunadamente, en la mayor parte del territorio español no existe consenso
en las medidas de gestión que compatibilizarían caza y agricultura. Por tanto, una de las
principales limitaciones para llevar a cabo programas de gestión efectivos es establecer
una coordinación entre ambos sectores. Esta coordinación entre sectores es realmente
difícil de lograr en buena parte de las pseudoestepas ibéricas, donde caza y agricultura
están completamente disociadas debido a intereses contrapuestos entre ambos gremios.
Este problema se agrava todavía más en terrenos donde la propiedad está muy dividida,
y en los cuales establecer nexos de unión resulta más complicado. Sólo cuando el
cazador puede controlar la gestión de la tierra puede ser viable establecer adecuadas
medidas de conservación. Por ello, es de vital importancia que la Política Agraria
13
Comunitaria (PAC), a través de las nuevas medidas de eco-condicionalidad, recoja e

integre todas aquellas propuestas que puedan mejorar el éxito reproductivo de la perdiz
roja, en especial aquellas medidas que no sólo puedan repercutir en beneficio de las
poblaciones de perdiz, sino que también puedan beneficiar a otras aves esteparias con
las que comparten su hábitat.
5.4. Sueltas de perdices de granja
En esta Introducción, ya se ha hecho referencia repetidas veces a la suelta de

perdices procedentes de granja tanto por el importante movimiento económico que
genera, como por su contribución (en un sentido u otro) a la recuperación de las
poblaciones naturales de perdiz roja. El negocio de la cría en cautividad de perdices
para sueltas ha alcanzado un volumen impresionante estimado entre 3-4,5 los millones
de perdices de granja que son liberadas cada año en España. Una elevada cifra, en
especial si se considera que poco más de 4 millones por año es el número estimado de
perdices cobradas en los últimos años (Gortázar et al. 2000; Baragaño & Otero 2001;
Blanco-Aguiar 2007). Si a todo esto añadimos la baja tasa de supervivencia (una vez
son liberados) de los individuos procedentes de la cría en cautividad (Gortázar et al.
2000; Alonso et al. 2005), nos encontramos ante una situación preocupante, ya que si
como estrategia de gestión, nos apoyamos en el número de individuos liberados para
establecer el cupo de capturas, podemos incurrir en un problema de sobreexplotación de
la población silvestre (Keane et al. 2005; Blanco-Aguiar 2007), que es especialmente
crítico en las poblaciones en declive (Blanco-Aguiar 2007).
Aunque la suelta de perdices de granja supone un importante recurso económico
que ha permitido mantener una pujante actividad cinegética alrededor de la perdiz roja,
a nivel ecológico, nos encontramos con una importante paradoja: la suelta masiva de
millones de ejemplares procedentes de granja podría ser incluso contraproducente para
recuperar las poblaciones silvestres. Por un lado, esta suelta masiva de una especie presa
como es la perdiz roja puede suponer un pequeño oasis para los depredadores, que
pueden encontrar en este tipo de aves un medio fácil de obtener alimento y
consecuentemente, ser otro problema adicional en la persecución ilegal de especies
amenazadas de depredadores (Viñuela & Villafuerte 2003). Por otro lado, la suelta de
perdices de granja podrían inducir problemas sanitarios tanto en la propia especie
liberada como en otras especies que comparten su hábitat, ya que con mucha frecuencia
14
Introducción
se liberan enormes cantidades de ejemplares en superficies reducidas, y a menudo con

parásitos o enfermedades que, además, son más propios de animales cautivos que de
fauna silvestre, y con los que no han tenido contacto previo (Millán 2004). De hecho,
recientemente se ha sugerido que la suelta de perdices puede estar transmitiendo
parásitos intestinales típicos de aves de granja, no encontrados anteriormente en los
sisones (Tetrax tetrax; Villanúa et al. 2007a) o diseminando en poblaciones naturales de
perdices parásitos intestinales típicos de granja (Villanúa et al. en prensa). Además, los
tratamientos sanitarios utilizados en granja para disminuir la carga parasitaria de las
aves antes de su liberación se muestran ineficaces (Villanúa et al. 2007b), lo que agrava
el problema potencial de transmisión de parásitos entre aves de granja y aves silvestres.
Este mismo problema podría estar produciéndose con otro tipo de parásitos o
enfermedades. En contraste con el problema de los parásitos intestinales, ampliamente
estudiado en los últimos años, existe una remarcable ausencia de conocimiento en lo
que a parásitos sanguíneos se refiere. La diseminación de las enfermedades causadas
por estos protozoos (géneros Plasmodium, Haemoproteus o Leucocytozoon) puede tener
importantes consecuencias en la dinámica poblacional de las aves, llegando incluso a
causar extinciones locales (Warner 1968; van Riper et al. 1986). Las perdices de granja
pueden tener elevadas prevalencias de parásitos sanguíneos (García, Pérez-Rodríguez &
Viñuela, datos inéditos). De hecho, el sistema de gestión de las perdices en granja
(grandes densidades y situaciones que favorecen un elevado grado de estrés), podría ser
particularmente favorable para la propagación de la malaria (García, Perez-Rodríguez &
Viñuela, datos inéditos). La información disponible sobre prevalencias o efectos de la
malaria en poblaciones silvestres de perdiz roja es escasísima (Encinas 1982; Little &
Earle 1995). Asimismo, las poblaciones naturales suelen tener menor resistencia a
parásitos con los cuales no han tenido contacto previo (Newton 1998), lo cual podría
repercutir en la supervivencia, condición física u otros parámetros biológicos de las
poblaciones silvestres. Hasta donde sabemos, no existe un tratamiento farmacológico
específico para los parásitos sanguíneos que sea usado para tratar las perdices en granja.
Por otro lado, nos encontramos con otro importante problema asociado a la
suelta de perdices de granja en el campo, la introgresión genética. De hecho, el riesgo de
alteración genética de las poblaciones silvestres de perdiz roja ocasionado por las
sueltas masivas es lo que mejor explica, junto con las profundas regresiones
demográficas de las poblaciones silvestres, que una especie cinegética de la que se
capturan millones de ejemplares cada año, éste considerada como vulnerable a nivel
15
mundial (Aebischer & Potts 1994). La maximización del rendimiento reproductivo

(mayores puestas) en las granjas y/o la competencia entre productores por obtener los
mejores precios, pudieron favorecer la práctica de la hibridación en granjas cinegéticas.
Incluso en el momento actual siguen existiendo híbridos en las granjas cinegéticas, dado
que no se ha generalizado ningún protocolo de análisis e inspección (Dávila, J.A., com.
pers.) y la suelta de estas perdices híbridas sólo ha sido declarada ilegal recientemente
(Blanco-Aguiar 2007). La hibridación mediada por el hombre se produjo sobre todo
entre la perdiz roja y la perdiz chukar (Alectoris chukar; Baratti et al. 2004; Barbanera
et al. 2005; Tejedor et al. 2007; Blanco-Aguiar 2007). Los híbridos de segunda
generación de estas dos especies son prácticamente indistinguibles de una perdiz roja
genéticamente pura (Negro et al. 2001), y las sueltas de perdices han extendido el
problema a las poblaciones silvestres. Aves híbridas se han detectado ampliamente
distribuidas por la península Ibérica, especialmente en áreas donde se han liberado
perdices con fines cinegéticos (Blanco-Aguiar 2007). También se han encontrado
híbridos en otras poblaciones (Baratti et al. 2004; Barbanera et al. 2005; Tejedor et al.
2007) y en todos los casos parecen tener un patrón común de origen humano (Blanco-
Aguiar 2007). La prevalencia de híbridos en el campo supone un grave problema para la
conservación de la “pureza” genética de la perdiz roja. Aunque hasta el momento la
mayoría de estudios realizados sobre la viabilidad de las repoblaciones indican que ésta
no es una medida de gestión efectiva (Gortázar et al. 2000; Perez et al. 2004), también
es conocido que las perdices de granja pueden llegar a sobrevivir y criar en el campo
(Duarte & Vargas 2004), lo que agrava más si cabe el problema sobre la permanencia y
cría de perdices híbridas en el campo. Urge por tanto evaluar que esta ocurriendo en el
campo con estas perdices híbridas.
6. Gestión agraria y cinegética como herramientas de conservación en la

pseudoestepa agrícola
La conservación de la diversidad biológica se ha ido convirtiendo poco a poco

en una prioridad social, supuestamente compatible con el uso racional de los recursos
naturales. En un medio donde caza y agricultura van prácticamente de la mano, y donde
la importancia de la caza es creciente, tanto por su componente socioeconómico como
por el carácter de utilización sostenible de unos recursos faunísticos, resulta
particularmente urgente la búsqueda de medidas de gestión que compatibilicen el
16
Introducción
aprovechamiento de ambas, sin afectar a la conservación de la diversidad biológica.

Para ello, la mejor forma sería utilizar la gestión agraria y cinegética como herramientas
de conservación para que ambas partes resulten beneficiadas.
Los esfuerzos realizados en la gestión cinegética de la perdiz roja están muy
extendidos (manejo del hábitat, control de depredadores, sueltas de perdices de granja,
aporte suplementario de agua y alimento en bebederos y comederos artificiales), de
forma que, junto con los aplicados en gestión agraria (concentración parcelaria,
mecanización, intensificación de los cultivos, cambios en la cosecha y agroquímicos)
son posiblemente los elementos más importantes que podrían afectar tanto a la
conservación de la perdiz roja como de las aves esteparias (Blanco-Aguiar et al. 2001;
Bota et al. 2005). Todas estas técnicas de gestión dirigidas a favor del mantenimiento de
las poblaciones de la perdiz roja podrían afectar positiva o negativamente a las especies
que coexisten en los mismos hábitats que pueden tener, hasta cierto punto, factores
limitantes y necesidades similares.
No hay que olvidar que en muchos casos la caza ha sido una actividad
tradicional que no sólo no ha repercutido negativamente en el estado de conservación de
determinados enclaves, sino que ha contribuido a que actualmente sean espacios
merecedores de protección legal por su excelente estado de conservación. Por tanto, la
actividad cinegética podría ser compatible con una política conservacionista
promocionando y financiando la preservación de los ecosistemas naturales, dentro de un
concepto de “uso sostenible”, siempre que se implemente una adecuada estrategia de
gestión, donde tengan cabida las actividades tradicionales humanas, la caza y la
conservación de la fauna silvestre (Lucio & Purroy 1992; Tapper 1999; Robinson &
Bennett 2004). Para ello se precisa de una gestión cinegética eficaz cuya meta sea
mantener poblaciones estables, genéticamente puras y en buen estado sanitario, al
tiempo que puedan ser rentables mediante un aprovechamiento cinegético sostenible.
Además, una buena gestión cinegética no sólo puede ser positiva para salvaguardar la
caza, sino que puede también reportar grandes beneficios para la conservación de los
hábitats y de las restantes especies no cinegéticas, incluidas las amenazadas. Por otro
lado, al igual que otras actividades de ocio, el desarrollo de la actividad cinegética
supone el uso compartido del espacio por humanos y fauna. El desarrollo de la caza es
una actividad que genera indirectamente un alto grado de perturbación en el medio y en
las especies que lo habitan (Madsen & Fox 1995; Fox & Madsen 1997; Tamisier et al.
2003; Duriez et al. 2005), ya sean tanto especies cinegéticas como otras con estatus de
17
conservación comprometido. Las reservas libres de caza podrían actuar en beneficio de

todas las especies presentes en el medio, mitigando en parte los efectos indirectos de
dicha actividad en el comportamiento y distribución de las aves. Por tanto, la regulación
de la actividad cinegética, así como la designación de una adecuada red de reservas,
podrían ser de gran ayuda para desarrollar estrategias de gestión conjuntas, de forma
que caza y conservación sean compatibles.
Objetivos
A lo largo de la introducción se ha mencionado en repetidas ocasiones la

importancia socioeconómica de la perdiz roja en nuestro país, sus peculiaridades
ecológicas y sus problemas de conservación. De entre estas características, es sin duda
su importancia socioeconómica (cinegética) la que hace de la perdiz una especie
diferente frente a otras aves de nuestra geografía. Sin embargo, en un medio donde se
explota más de un tipo de recurso (caza y agricultura), como es el caso de las
pseudoestepas agrícolas, se hace necesario el desarrollo de una estrategia de gestión
conjunta, para lo cual es necesario conocer el efecto de las diferentes prácticas de
gestión sobre la especie. Por otro lado, dentro de las estrategias de gestión cinegética, en
esta tesis doctoral nos hemos centrado en investigar uno de los aspectos de mayor auge
en los últimos tiempos: la suelta de aves procedentes de granja. Por último, estudiar el
efecto indirecto (perturbación y uso del espacio) sobre las aves del desarrollo de la
actividad cinegética es una pieza necesaria para completar la información en estos
medios. El objetivo general de esta tesis doctoral es evaluar de forma conjunta el efecto
de la gestión cinegética y agrícola principalmente sobre las poblaciones de perdiz roja,
tratando de integrar toda esta información y desarrollar estrategias de gestión y
aprovechamiento compatibles con la conservación del medio, sus especies y el
desarrollo de las actividades humanas. En conjunto, la comprensión de dichos procesos
puede ayudar a desarrollar nuevas estrategias de gestión conjuntas entre cazadores y
agricultores, que permitan que distintos aprovechamientos como la agricultura, la caza y
la conservación sean compatibles y factibles, sin prejuicio del resto de especies que
comparten el mismo hábitat.
Como se ha indicado anteriormente, a pesar de la importancia socioeconómica y
ecológica de la perdiz, aún existen ciertas lagunas de conocimiento sobre su biología
reproductiva. Dentro del marco mediterráneo las especies están sometidas a una alta
18
Introducción
variabilidad climatológica interanual, ante la cual pueden adoptar distintas estrategias

reproductivas para maximizar su esfuerzo reproductivo sin hipotecar su futura
supervivencia. Esta información es vital antes de desarrollar cualquier estrategia de
gestión. Así pues, el primer objetivo de esta tesis es conocer los factores que pueden
influir en la reproducción (doble puesta, tamaño de puesta y éxito de eclosión) de la
perdiz roja (capítulo 1), en su hábitat principal y donde alcanza mayores densidades, las
pseudoestepas ibéricas.
Por otro lado, la pseudoestepa es un medio sometido a un intenso y continuo
manejo del hábitat, donde la escasez de lugares adecuados para la nidificación de las
aves es un factor limitante. Sin embargo, en una zona donde el aprovechamiento
agrícola no es el único que se obtiene de la tierra, esto puede significar que junto con la
gestión agrícola, la gestión cinegética suponga otro de los factores que influyan en el
éxito de nidificación de la perdiz roja. Por tanto, el segundo objetivo sería conocer el
hábitat de nidificación de la perdiz roja y comprobar los efectos de la gestión cinegética
y la gestión agrícola sobre el éxito de nidificación de la perdiz en medios agrícolas
(capítulo 2). Este es un factor importante para determinar la relevancia en el éxito
reproductivo de ambos sistemas de gestión. Además, esta información puede resultar de
utilidad para otras especies que comparten el mismo hábitat.
La suelta de perdices procedentes de granja es un fenómeno muy extendido, y
algunos de los posibles efectos que se podrían derivar de tal actividad aún no están bien
explorados. La hibridación artificial de la perdiz roja con la perdiz chukar para mejorar
los rendimientos productivos en las granjas, y la posterior suelta de éstas al medio, han
extendido el problema a las poblaciones silvestres, amenazando la conservación de la
pureza genética de la perdiz roja. Sin embargo, poco se sabe del papel que pueden estar
jugando estás perdices híbridas en la naturaleza. Por ello, el tercer objetivo es
investigar las consecuencias de la introgresión genética (hibridación con Alectoris
chukar) en el fenotipo y en la eficacia biológica en poblaciones silvestres de perdiz roja
(capítulo 3). Evaluar las diferencias en tamaño corporal, condición física, parámetros
reproductivos, supervivencia y causas de mortalidad entre híbridos y no híbridos, podría
ayudar a conocer la magnitud del problema y determinar cuál puede ser la mejor
estrategia para solucionarlo.
Igualmente las sueltas de perdices pueden inducir problemas a nivel sanitario.
Los parásitos intestinales de perdices procedentes de granja y de perdices silvestres
difieren sustancialmente. Sin embargo, poco se sabe sobre los parásitos sanguíneos. El
19
interés de las relaciones parásito-hospedador y sus efectos sobre las poblaciones

silvestres de animales están actualmente siendo objetivo de estudio de muchas
disciplinas tales como la biología evolutiva, ecología, parasitología, etología, gestión de
la vida silvestre y biología de la conservación. Además, los cambios inducidos por los
humanos en el medio ambiente podrían alterar la estructura genética espacial de ambos,
parásitos y hospedadores. No obstante, las especies que habitan medios abiertos como
en nuestro caso, suelen tener bajas prevalencias de parásitos sanguíneos. La suelta de
perdices procedentes de granja podría alterar esta estructura espacial. El cuarto
objetivo es determinar la prevalencia de los parásitos sanguíneos en una especie
habitante de medios pseudoesteparios, así como los parámetros geográficos y las
implicaciones de la gestión cinegética que pudieran condicionar la distribución y
presencia de los parásitos (capítulo 4).
Por último, el incremento de las actividades de ocio humanas ha amplificado las
potenciales consecuencias de la perturbación humana en la fauna silvestre. La caza es
una de las actividades humanas que más afecta a la vida silvestre, y que además recibe
una creciente atención dada su dimensión social y económica. La mayoría de estudios
sobre los efectos de la caza en la fauna silvestre se han llevado a cabo en zonas húmedas
o costeras. La actividad cinegética puede afectar tanto a la distribución como al
comportamiento de las aves y tener costes en la eficacia biológica. Para tratar de paliar
estos efectos, en distintos países de Europa se han establecido una serie de zonas
protegidas, donde la caza no esta permitida y que no suelen ocupar más de un 10 % de
la superficie del coto de caza. Tomando como ejemplo el diseño de áreas libres de caza
establecido en Francia en hábitats agrícolas, el quinto objetivo es evaluar el efecto de la
actividad cinegética en el comportamiento y el uso de las reservas de caza en especies
de interés cinegético (aunque de menor interés como avefría y chorlito dorado) y de
especies de interés de conservación (sisón común) (capítulo 5). Comprobar el papel que
pueden jugar las reservas de caza es crucial para la gestión de las especies cinegéticas y
para la conservación de especies amenazadas en áreas agrícolas.
Con la integración de la información obtenida de los cinco objetivos propuestos,
se pretende proponer una serie de medidas e ideas que ayuden a mejorar la gestión
cinegética de la perdiz roja y la conservación de otras aves esteparias protegidas.
Además, esto permitiría proponer importantes herramientas para mejorar la gestión
agraria que favorezcan, tanto a las poblaciones de aves objeto de estudio como a las que
comparten su hábitat.
20
Introducción
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29
CAPÍTULO 1
Doble incubación, variación en el tamaño de puesta y éxito de eclosión

en la perdiz roja Alectoris rufa: Nueva información dentro de un
peculiar sistema de reproducción en aves
Casas, F. Mougeot, F. & Viñuela, J. Double brooding, clutch size variation, and hatching
success in wild red-legged partridges Alectoris rufa: novel insights into a peculiar avian
breeding system. Behavioural Ecology, en evaluación.
Capítulo 1
ABSTRACT
1. The evolution and regulation of offspring number, parental care, and breeding
systems is a classical study area in ecology that has received major attention in
the literature. Double brooding behaviour could be considered an intermediate
stage in the evolutionary trend from biparental to uniparental care of single
clutches. Regulation of clutch size and hatching success could determine the
viability of a double clutching behaviour or male uni-parental care systems.
2. The red-legged partridge Alectoris rufa is a game bird with high productivity
exhibiting a peculiar breeding system of double nesting behaviour. Females
often lay eggs in two different nests, one incubated by the female, and the other
one by its male. The main aim of this study was to collect data on the breeding
ecology of red-legged partridges in central Spain, in the core area of the species,
and in its most important habitat, the “agrarian pseudosteppes”, where partridges
achieve their highest densities.
3. This study is the first performed in a long series of years, with contrasting
environmental conditions, allowing an examination of the factors affecting the
occurrence and success of double clutching behaviour, a critical information to
understand this breeding system that has not been provided up to now. We also
examine the factors affecting clutch size and hatching success, and how these
relate to the sex of the incubating bird, laying date, year and hunting
management models.
4. The probability of incubating significantly differed between sexes, but only the
proportion of males that incubated varied markedly between years. This effect
was mainly due to year 2005, when no male incubated. Females showed similar
incubation rate all study years. Variation in laying date was explained by year
and by the sex of the bird incubating, depending on year. Laying occurred earlier
in 2003 than in other years. Clutches incubated by males were laid earlier than
those incubated by females in this year of early laying, but later in 2004, the year
when laying was more delayed.
5. Clutch sizes varied significantly among years and between sexes. Average
clutch sizes were largest in 2003 and 2007, and smallest in 2005. Clutches
incubated by males were larger than those incubated by females. Clutch size also
decreased with increasing laying date, similarly so in both sexes. The probability
of a clutch being lost to predators differed between sexes, being higher for nests
incubated by females. Variation in hatching success was explained by year and
sex. Hatching success was lowest in 2007. Clutches that were laid late and
incubated by males had a lower hatching success.
6. Synthesis and applications. We failed to found differences in all the breeding
patterns explored among hunting management models, the simplest explanation
is the lack of effect of hunting management in the breeding ecology of
partridges, most likely more influenced by inter-annual variations in weather
conditions and food availability. Females laid more eggs in years when spring
rainfall was high, and males contributed more to incubation in those years. In a
dry year, males do not incubate. We discuss our results within the context of the
evolutionary origin of uni-parental care in birds, clutch size, hatching success
and the main factors affecting double brooding occurrence.
33
INTRODUCTION
The evolution and regulation of offspring number, parental care, and breeding
systems is a classical study area in ecology that has received major attention in the
literature (Skutch 1982; Winkler & Walters 1983; Martin 1987; Clutton-Brock 1991;
Ligon 1999). In most endotherm animals with internal fertilization, females are the sex
devoting more investment to offspring rearing, often without any help by her mates
(Clutton-Brock 1991). Birds are an exception, since about 80 % of species provide bi-
parental care to offspring, although females are usually the sex devoting more
investment (Lack 1968; Cockburn 2006). An intriguing exception to the general rule of
higher female investment is also found among birds, since in a small group of species
(c. 1 %; mainly precocial species within ratites and charadriforms), males are the main
providers of parental investment, taking charge of incubation and post-hatching chick
care (Lack 1968; Cockburn 2006). The evolutionary origin or functional basis of this
interesting reversal in sexual roles has remained a puzzling question in evolutionary
biology for decades (Lack 1968; Clutton-Brock 1991; Ligon 1999; Owens 2002;
Cockburn 2006). Somehow in between of these opposed patterns of parental care there
is another small group of bird species with double brooding behaviour: both male and
female incubate and take care of chicks simultaneously or sequentially in the same
breeding season (cases within charadriforms and galliforms; Green 1984). This system
could be considered an intermediate stage in the evolutionary trend from biparental care
of single clutches to male- or female-only uniparental care of single clutches (or
viceversa, depending on the ancestral state in the phylogeny), the most common
evolutionary transition detected by phylogenetic analyses (Owens 2002; Reynolds et al.
2002; Cockburn 2006). The discussion about the origin of uniparental breeding systems
is often based on “which sex deserts the other at the nest” (Owens 2002), but double
brooding is a system apparently requiring “mutual confidence” of sexes. For example,
the male caring a first clutch while his mate lays a second one without mate guarding
(Pierce & Lifjeld 1998), or the female trusting that her mate is going to incubate a
clutch instead of deserting and looking for new mates (Green 1984). Thus, improving
our knowledge of the evolutionary and functional meaning of this double brooding
system can contribute to our global understanding or the old unresolved problem of
reversed sexual role in breeding of birds.
34
Capítulo 1
Intimately linked to the problem of double clutching behaviour, or to the origin

of uniparental male care breeding systems, is another contentious issue in evolutionary
ecology, such as the regulation of clutch size (Green 1984; Cutton-Brock 1991; Ligon
1999; Smith & Hardling 2000; Owens 2002). It is already clear that birds can rear more
young than the number of eggs they lay (Monaghan & Nager 1997), contrary to Lack’s
predictions (Lack 1947), but also that there may exists a trade-off between parental
investment in reproduction and self-maintenance (Clutton-Brock 1991). Clutch size
variation has long been attributed to food limitation rather than to nest predation in
northern temperate climates birds (Roff 1992), although predation may explain clutch
size variation within latitudes (Martin & Clobert 1996). Precocial birds such as the red-
legged partridge Alectoris rufa have relatively minor reproductive costs as compared to
altricial species, due to early feeding autonomy of chicks. Galliforms in general are
among the birds able to lay a higher number of eggs within a breeding season (Lack
1968), and it has been questioned why no more species exhibit a double clutching
behaviour (Green 1984). Finally, a basic functional link between double brooding
behaviour and clutch size is hatching success, as a main trait determining fitness, and
thus viability of a double clutching behaviour or male uni-parental care systems
(Fernández & Reboreda 2007).
The red-legged partridge is a game bird with high productivity exhibiting a
peculiar breeding system of double nesting behaviour (Cramp & Simmons 1980; Green
1984). Male incubation behaviour varies among species of the genera Alectoris, but is
only common in the red-legged partridge (Cramp & Simmons 1980; Vavalekas et al.
1993; Green 1984) and little is known about this breeding strategy. Females lay eggs in
two different nests, and when both clutches are laid, females usually start incubation the
second and males incubate the first-laid clutch (Green 1984). This breeding system may
be shaped by a complex pool of trade-offs in male and female behaviour. Incubating
males would restrict their time available for other activities, such as foraging or
attracting additional mates (Reid et al. 2002). Time spent incubating may reduce the
opportunity for males to obtain additional mates or extra-pair copulations (EPC). Extra-
pair paternity (EPP) rates are generally low in species where males contribute
extensively to incubation (Schwagmeyer et al. 1999). Red-legged partridges are often
considered as socially monogamous (Del Hoyo et al. 1994), but EPPs cases of polyginy
have been recently documented (Casas et al. 2006b), as well as a high divorce rate and
frequent mate change during early breeding season (Mougeot et al. in prep.). The
35
traditional assignment of red-legged partridge to monogamy probably has not been

based on rigorous research, but on the common observations of apparently tight social
association between sexes, which might reflect intense mate guarding rather than real
monogamy (Westneat et al. 1990, Griffith et al. 2002).
In this context of a complex mating system, males would face a trade-off
between paternal investment, attraction of new mates and engagement on EPPs (e.g.
Veiga et al. 2002; Cordero et al. 2003). Additionally, since incubation may commonly
be a period of time and energy limitation in birds (Deeming 2002), and a period of high
predation risk for adults (e.g. Potts 1980), paternal investment in incubation could affect
future survival. It has been shown that the costs of breeding for males taking charge of
clutches in precocial species can be high (Holt et al. 2002; Fernández & Reboreda
2003). Therefore, males could follow two kinds of strategies, incubating and rearing
chicks or attracting additional females. The parameters determining why a male takes
one way or another could be several, such as breeding status (mated, divorced or
single), mate quality, body condition, laying date, population density and sex-ratio
influencing opportunities for EPPs, (Green 1984; Clutton-Brock 1991; Blomqvist et al.
2001; Owens 2002; Cockburn 2006). However, it is important to consider that male
incubation could be intimately tied to the physiological ability of females to lay two
clutches. It is obvious that laying eggs in two different nests is a female decision at the
root of the double brooding strategy. Nest abandonment may be relatively common in
red-legged partridges (Green 1984; Rueda et al. 1993), and it is considered a key trait to
explain variation in breeding systems of birds (Owens & Bennett 1997; Owens 2002).
Females may be particularly exposed to the problem of abandonment by males after
copulation (Owens 2002), what could be the origin of female uni-parental care systems.
Thus, females take a risk of loosing their investment when leaving a clutch under the
care of their mates.
The main aim of this study was to collect data of the breeding ecology of red-
legged partridges in central Spain, with special reference to the factors influencing
double clutching behaviour, and studying variation of two key elements of breeding
ecology such as clutch size and hatching success. This study is the first performed over
several years, with contrasting environmental conditions, allowing an examination of
the factors affecting prevalence and success of double clutching behaviour, a critical
information to understand this breeding system that has not been provided up to now.
Furthermore, the study was performed at the core area of the species and in its most
36
Capítulo 1
important habitat, the “agrarian pseudosteppes”, where partridges achieve their highest
densities (Blanco-Aguiar et al. 2003; Vargas et al. 2006), while the most important
work performed up to now was conducted on an introduced population established in a
sub-optimal area (Green 1984). We examine the factors affecting double clutching
occurrence, clutch size and hatching success, and how these relate to sex, laying
beginning date, year and hunting management models. We discuss our results within the
context of the evolutionary origin of uni-parental care. Furthermore, the red-legged
partridge is a game bird with high socioeconomic value, and research on factors
regulating breeding ecology in natural populations may help managers to develop
management tools for improving productivity.
MATERIAL AND METHODS
Study area
The study area covered 125 km² and was located in Campo of Calatrava (Central
Spain, 38º 80´ N, 3º 80´ W, 610 m a.s.l.). This is an undulated farmland area dominated
by a mosaic of crops, mainly cereal (particularly barley), with interspersed patches of
olive groves, vineyards, and a few patches of dry annual legume crops (mainly vetch
Vicia sativa) and sugar beet Beta rubra. Natural vegetation areas are very scarce,
including just some small areas of short scrubland and pastureland mainly limited to the
rocky top of hills. Other crops, ploughed or abandoned farmland, and urban areas
(mainly country houses) cover less than 10% of the area.
The study area included four game estates, characterised by three different
hunting management models (hereafter “sites”; see chapter 2 and 4).
Data Collection
Captures, radio-tracking and nest monitoring
We conducted the fieldwork in 2003-2005 and in 2007, in spring and early

summer (February to June). Over the four years, we caught 135 adult partridges in
February-March (39 in 2003, 44 in 2004, 32 in 2005 and 44 in 2007). For the period
2003-2005, we used cage traps with adult alive partridges inside the cages as a decoy to
37
catch partridges. Traps were baited with wheat to attract partridges. In 2007, birds were
caught at night, by lamping and netting them with a hand-held net, and by locating
roosting birds with a powerful head-torch or using an infra-red camera (Panatec;
Madrid, Spain).
All captured birds were sexed from plumage, biometry and ornaments (Sáenz de
Buruaga et al. 2001). We also took a blood sample from the brachial vein (0.5-1 ml) to
confirm the sex of birds using genetic analyses of blood samples (authors, unpublished
data). Each bird was fitted with a necklace radio-transmitter with mortality sensor
(BIOTRACK, 10 gr.), and released at the capture site. After capture, we located birds
every 1-5 days by radio-tracking, using AOR-AR8200 multiband receptors and three
element YAGI antennas. We located and visited nests using radio-tracking, when birds
were found on several consecutive days at the same location. All analyses were carried
out exclusively with first clutches, excluding replacement clutches (n=5).
We first determined for each nest the onset of incubation (± 2 days). This was
done either from (1) daily radio-tracking allowing us to determine the exact day when
incubation began (in 2003-2005, and most nests in 2007), or (2) by estimating the day
incubation started from egg density (some nests in 2007; we established the daily egg
density loss of incubated eggs, and estimated for how many days eggs had been
incubated given their measured density during the nest visit; unpublished data), or (3)
backdating from known hatching date (considering that incubation lasts 24 days and
that it starts after laying of the last egg; Del Hoyo et al. 1994; Cabezas-Díaz & Virgós
2007), when nests were visited during hatching or when the day the radio-tagged bird
left the nest with recently hatched chicks was known.
Table 1. Year, nest separation distance, clutch size and incubation beginning date (1= 1st April) of radio-
marked pairs of Red-legged partridges with two nests simultaneously active.
Nest Clutch Size Incubation Beginning

Separation Date
Pair Year (m) Male Female Male Female
1 2004 76 12 10 53 43
2 2007 381 14 11 43 37
3 2007 314 17 12 47 41
4 2007 96 16 14 61 40
38
Capítulo 1
Females lay eggs every two days on average (Cabezas-Díaz & Virgós 2007), so
we estimated laying dates as the day incubation started, minus the final clutch size
multiplied by 2 days. Laying dates were indexed relative to the 1st of March (day 1).
We determined hatching success by visiting nests soon after hatching was
detected (1-2 days).
Statistical Analysis
Differences in incubation rate between the sexes
Female red-legged partridges may lay two clutches, the first usually incubated
by the male and the second by herself (Green 1984). Bearing this in mind, we calculated
a “nest incubation rate”, defined as the percentage of radio-tagged individuals of each
sex that began to incubate a nest, independently of final nest fate. Individuals that died
before incubation (n =22 females, n =18 males) were excluded from these analyses. We
performed a first analysis of the nest incubation rate by sex starting by a saturated
Generalized Linear Model (GLMz) with binomial error distribution and logit link
function, subsequently following a backward stepwise procedure (Crawley 1993), with
the dependent variable “incubation” (0=no incubation; 1=incubation), and sex as
explanatory variables. Model fitting was assessed by Akaike’s Information Criterion
(Burnham & Anderson 1992), and the level of significance was established at 5 %.
After detecting differences between sexes, we performed a second GLMz analysis for
each sex separately, with year and sites as independent variables following the same
procedure.
Clutch size
Determination of overall clutch size of female red-legged partridges is a difficult

task, because they may lay eggs in more than one nest, usually two, one incubated by
his mate, and the other by herself (Green 1981, 1984). The only way to precisely
determine the overall number of eggs laid by a female is monitoring simultaneously
both members of the pair. From 2003 to 2005, the capture method (cage traps), was
little successful for catching both pair members (16 complete pairs caught). In 2007, we
changed the capture method, improving our success (18 complete pairs caught). Even so
39
we still had problems to estimate the real number of eggs laid per female, because we
found a high rate of divorce or mate change during the period between capture and
incubation (Mougeot et al. in preparation), cases of mate loss to predation or failures in
transmitters. Finally, we obtained complete data sets for only four tabbed pairs (Table
1). Moreover, we also know that intraspecific nest parasitism or polygamy is relatively
common in this species (Casas et al. 2006a, b). For all these limitations, we have only
considered clutch size of each individual nest, but we acknowledge that this does no
accurately reflect the real laying effort of each female. However, given that our main
objective was to study inter-annual variation in clutch size, and taking into account that
during incubation, the energy requirements increase with increasing clutch size (Ward
1996; Williams 1996), this may be an reasonable estimate of incubation ability and
parental effort.
We explored the sources of variation in clutch size by using a General Linear
Model (GLM) with normal error function and identity link function, considering “clutch
size” as a continuous dependent variable, and date of laying onset, sites, sex and year as
independent variables. In this analysis, we considered all nests (n=65) for which we
knew final clutch size, excluding cases in which the clutch was lost during laying or in
which the final clutch size was not recorded. Due to the differences between years in
field work effort carried out on the various sites, and the unbalanced sample sizes
among sites, we excluded “a priori” from the analysis all the interactions with this
variable. We initially included all remaining two-way interactions, and followed the
same procedure described above. We used a Tukey post hoc test, to determine
significant differences among groups. To allow comparisons, laying beginning date was
encoded as to March 1 equal to day 1 for all study years.
Hatching success
Because we were interested in natural variations in nesting success, we excluded

from our analyses clutch losses due to agricultural practices (n = 13) or poaching (n =
3), that have been presented elsewhere (chapter 2). In this subsample, we first analysed
the probability of clutch being lost to predation of the incubating birds or the whole
clutch. Predation probability was fitted to GLMz models using a binomial error
distribution and a logit link function.
40
Capítulo 1
Second, we analysed variation in hatching success, excluding clutches that were

entirely lost (agricultural practices, predation, or other nest loss causes). For these
analyses, we considered only successful nests (n=34), and adjusted data by GLMz with
poisson error distribution and log link function, following a backward stepwise
procedure (Crawley 1993). Due to the small sample size, we first checked that there was
no significant effect of hunting management models, because we were more interested
in annual variation, and all game states in the study area had similar natural conditions
in an overall area of about 12.5 km² (see chapter 2). We considered the effects of
laying date, sex and year in a GLMz analysis, following the same procedure described
above.
All the analyses were performed with the statistical package STATISTICA 6.0
and SAS 8.01 (SAS 2001).
RESULTS
Proportion of females and males incubating
The probability of incubating significantly differed between sexes (χ² = 28.7, df

= 1, P < 0.001). 94.66 % of radio-tagged females (n = 50) incubated, whereas only
40.97 % of radio-tagged males (n = 49) did so. The proportion of females incubating did
not differ significantly between years (χ² = 1.07, df = 3, P = 0.78; Fig. 1a) or sites (χ² =
1.01, df = 2, P = 0.6). In contrast, the proportion of males that incubated varied
markedly between years (χ² = 10.46, df = 3, P = 0.0053; Fig. 1a), but not between sites
(χ² = 2.78, df = 2, P = 0.24). This effect was mainly due to year 2005, when no males
incubated at all, while the proportion of males incubating the other three years was
fairly similar (Fig. 1a).
Laying dates: differences between years and between nests incubated by females
or males
Variation in laying date was not significantly explained by site (F2,63 = 1.88; P =
0.161), but was explained by year (F3,59 = 5.14; P = 0.003) and by the sex of the bird
incubating, depending on year (sex: F1,59 = 1.60; P = 0.211; sex × year interaction: F2,59
= 3.16; P = 0.049). Laying occurred earlier in 2003 than in other years (Fig. 1b).
41
Clutches incubated by males were laid earlier than those incubated by females in this
year of early laying, but later in 2004, the year when laying was more delayed (Fig. 1b).
In the four tabbed pairs of our sample (Table 1), males always started incubation later
than females (Green 1984), but unfortunately, no data are available for any tabbed pair
on the year 2003, when we detected that females began incubation much after than
males.
Incubated by females
Incubated by males
100
Proportion incubating
80
60
a)
40
20
0
80
6
70 8
6
13
Laying date
16 10
60
b)
50 7
40
30
16
14
Clutch size
c) 12
10
1.0
Hatching success
0.8
d) 0.6
0.4
0.2
0.0
2003 2004 2005 2006 2007
Year
Figure 1. Inter-annual variations in: a) proportion (%) of birds incubating; b) mean ± SE laying date (1 =
1st of March); c) mean ± SE clutch size (number of eggs) and d) mean ± SE hatching success (proportion
of eggs hatched, excluding clutch losses due to predation) according to the sex of the incubating bird
(white dots (○): females; black dots (●): males).
42
Capítulo 1
Clutch size
Clutch sizes did not differ significantly between sites (F2,59 = 0.40; P = 0.669),
but varied among years (F3,59 = 4.99; P = 0.004), and between sexes (F1,59 = 8.70; P =
0.005). Average clutch sizes were largest in 2003 and 2007, and smallest in 2005 (Fig.
1c). Clutches incubated by males were larger than those incubated by females (12.66 ±
0.69 and 10.06 ± 0.47, respectively; all years combined). Between-sexes differences in
clutch size were significant in 2003 (F1,21 = 6.14; P = 0.022), marginally significant in
2007 (F1,21 = 4.08; P = 0.056), but not significant in 2004 (F1,10 = 0.39; P = 0.547; Fig.
1c).
Clutch size also decreased with increasing laying date, similarly so in both sexes
(model controlling for year and sex; laying date: F1,59 = 54.29; P < 0.001; sex × laying
date interaction: F1,59 = 0.49; P = 0.485; Fig. 2).
Incubated by males
25
20
15
Clutch size
10
0
0 20 40 60 80 100
Laying date
Figure 2. Relationship between laying date and clutch size (white dots (○): nests incubated by females;
black dots (●): nests incubated by males).
Hatching success
Clutch losses due to predation. The probability of a clutch being lost to

predators did not differ between sites (χ² = 0.78, df = 2; P = 0.676) or years (χ² = 3.26,
43
df = 3; P = 0.353), but differed between sexes (χ² = 7.99, df = 1; P = 0.005). Total losses
due to predation occurred in 40.0% of nests incubated by females (n = 30), but only in
5.6% of nests incubated by males (n = 18).
Unhatched eggs. We further analysed hatching success variation using clutches

that reached hatching stage. Variation in hatching success was not explained by site (χ²
= 2.28, df = 2; P = 0.320), but was explained by year (χ² = 9.24, df = 3; P = 0.026) and
sex (χ² = 3.26, df = 1; P = 0.045), the interaction year × sex being not significant (χ² =
1.32, df = 2; P = 0.516). Hatching success was lowest in 2007 and was lower for nests
incubated by males (Fig. 1d).
Incubated by males
1.2
1.0
Hatching success
0.8
0.6
0.4
0.2
0.0
10 20 30 40 50 60 70 80
Laying date
Figure 3. Relationship between hatching success (proportion of eggs hatched, excluding clutch losses due
to predation) and laying date according to the sex of the incubating bird (white dots (○): females; black
dots (●): males).
For nests incubated by females, hatching success did not differ significantly
between years (χ² = 0.48, df = 3; P = 0.923; Fig. 1d) and did not vary with laying date
(lay date: χ² = 0.00, df = 1; P = 0.957; lay date × year interaction: χ² = 2.23, df = 3; P =
0.526; Fig. 3) or with clutch size (χ² = 0.10, df = 1; P = 0.757). In contrast, for nests
incubated by males, hatching success differed between years (χ² = 21.48, df = 2; P =
0.001; Fig. 1d) and decreased with increasing laying date (χ² = 26.58, df = 1; P < 0.001;
Fig. 3) and with clutch size (χ² = 9.73, df = 1; P = 0.002), the interaction year × laying
44
Capítulo 1
date being not significant (χ² = 3.05, df = 2; P = 0.217). Clutches that were larger, laid
late and incubated by males had a lower hatching success (Fig. 3).
DISCUSSION
Which are the main factors affecting double brooding occurrence?
We estimated male incubation rate with regard to the total number of males that
we had radio-tagged, instead of using the number of nests located (see Green 1984). Our
data are therefore the first ones giving a picture of the proportion of males who take
charge of the care of a clutch in a natural red-legged partridge population, in the original
distribution area of the species. We found that almost all females surviving until late
breeding season incubated a clutch independently of yearly conditions, while the
proportion of males incubating was highly variable among years, from none in one year,
to c. 50 % in the other three study years. Furthermore, nests incubated by males had
larger clutches and lower losses due to predation or farming activities (chapter 2) than
those incubated by females, a result that stresses the importance of male contribution to
partridge reproductive success.
Table 2. Weather conditions during the study period. Winter (22nd December to 21st March) and spring
(22nd March to 21st to June). Temperature (ºC) calculated as average for each period, humidity (% water
saturation) calculated as average for each period; and rainfall (l/m2) calculated as the accumulation for
each period. (Data take out from agrometeorological station of Ciudad Real of the SIAR, Servicio Integral
de Asesoramiento al Regante http://crea.uclm.es/~siar/webphp/resu_hist.php).
Temperature Humidity Rainfall

2002-2003 winter 5.99 79.93 149.8
2003 spring 13.22 64.27 158.2
2003-2004 winter 5.98 82.01 116.4
2004 spring 10.71 72.46 78.4
2004-2005 winter 3.48 72.24 50
2005 spring 13.42 54.9 98
2006-2007 winter 5.31 83.55 66.6
2007 spring 11.41 68.98 203.8
No males were found incubating clutches in 2005, a year of marked drought in

our study area (Table 2), in which vegetation growth, including cereal, was poor. In that
year, laying occurred very late and we found the smallest clutch sizes. This result
suggests that the ability of females to lay a large clutch early in the season may be the
first and most important factor determining if males incubate a brood in a partridge
45
population (Green 1984), particularly taking into account that in other years, we found
that late nests incubated by males had poor hatching success (Fig. 3).
We also found a marked year-to-year variation in the laying dates of nests
incubated by males or females. In the two years with apparently the best breeding
conditions (2003 and 2007), laying dates of nests incubated by males were earlier or
similar than those of females. In contrast, the opposite was found in 2004, a year with a
drier spring (Table 2), in which partridges laid relatively small clutches late in the
season. This results suggest that, under good breeding conditions, females lay eggs
early, and males take charge of the first clutch soon after finished, while under poorer
conditions females would start first their own clutch. Green (1984) reported that males
usually incubate the first clutch laid by females, but also found cases of females
incubating the first clutch (17%). Perhaps in years with relatively poor breeding
conditions, females start a clutch to be incubated by her mates later than her own, while
in good years they would be more prone to leave a first clutch under the care of their
mate. These different strategies could be associated to laying dates, because nests
incubated by males late in the season have poor hatching success (see below).
Alternatively, males could also be more prone to start incubation earlier in good years,
and females would adjust their behaviour to their expectancies about male behaviour.
Interestingly, variations in breeding systems between species or populations of waders
also seem to be related to the timing of laying (Blomqvist et al. 2001).
Predation has been considered to be a major force driving double brooding
behaviour in partridges (Green 1984). Climatic variation in mediterranean ecosystems
could affect nest predation probability through differential vegetation growth (Díaz &
Carrascal 2006; Pescador & Peris 2007), which is known to affect predation
probabilities of partridges’ nests (Ricci et al. 1990). Thus, it could be expected that
partridges would adjust their behaviour to perceived nest predation risk. However, we
did not find significant variation among years in nest predation rates, which were
overall very low for males’ nests. Furthermore, on the year in which vulnerability of
nests to predation should have been higher due to scarce vegetation (2005), males did
not incubate nests. Thus, our results do not support the hypothesis that females would
be more willing to leave a clutch to their mates in a context of high predation risk.
In any case, even in good breeding years, we still found a high percentage of
males that did not incubate. In fact this proportion was surprisingly similar in the other
three study years, about 50 %. Further research is needed to accurately determine the
46
Capítulo 1
constraints that control this behaviour, which seems to be a female decision that might
be based on its perception about future commitment of males to attend its clutch.
Clutch Size
Lucio (1990) pointed out the strong influence of climatic conditions on red-
legged partridge productivity considering only chick survival rates, but without any
information on clutch size or laying dates. We found large differences in clutch size
among years in the direction pointed out by Lucio (1990), with smallest clutch sizes and
no double brooding in 2005, a year with marked drought in late winter and spring
(Table 2). Rueda et al. (1993) reported a similar trend for reduced clutch size in a dry
year, in another study area in Central Spain. These results suggest, first, that females
could have experienced a physiological limitation during laying, probably related to low
food availability (Monaghan & Nager 1997; Tortosa et al. 2003; Lepage & Lloyd
2004), and, secondly, that male incubation must be intimately tied to the physiological
ability of females to lay two clutches. A main trait of Mediterranean climate is the high
inter-annual variability and unpredictability of temperature and rainfall regimes
(Blondel & Aronson 1999). Late winter and spring rainfall is critical for plant growth,
environmental productivity and thus food supply (Peinado & Rivas-Martínez 1987,
Lucio 1990). Female ability to produce eggs probably depends on available resources
and could be subject to large interannual variations (Cattadori et al. 1999; Watson et al.
2000). However, little is known about spring diet of partridges in Spain (Rueda et al.
1992), and nothing about the possibility of food shortage in natural conditions. Thus,
alternative explanations to food limitation constraint cannot be ruled out. For example,
in a year of drought, concentrating the breeding effort on smaller single clutches could
be a more successful strategy if predation risk is increased due to low vegetation cover.
Vegetation cover is a key factor for nesting success in this species (Ricci 1985; Rands
1987; Ricci et al. 1990). In dry years, vegetation development is reduced, leaving nests
more exposed to predation during laying and incubation. Smaller clutches are exposed
to predators for shorter time and may thus be the best option to ensure breeding success
under conditions of high predation risk (Skutch 1982; Green 1984). Nest predation rate
was slightly higher in the dry year, although differences were not significant (see also
chapter 2), and with our methodology to detect nests, we could be underestimating the
frequency of clutches lost to predators before the onset of incubation. Clutch size also
47
declined along breeding season, a general rule in birds (Martin 1987), including
precocial species (Winkler & Walters 1983), a trait that could also be mediated by food
abundance or by a high predation risk. Additionally, we cannot discard that other
population parameters not considered in this study, and perhaps affected by weather,
such as population density (Mougeot et al. 2003), parasite prevalence (Millán et al.
2002), or age structure (Green 1984; Cabezas-Díaz et al. 2005), could influence
breeding rates, as reported in other galliforms (Cattadori et al. 1999).
Clutches incubated by males were larger than those incubated by females, and
this was consistently observed across years. This is a result contrasting with the study
by Green (1984), who did not find such sex-related differences in clutch size. Again,
this should be mainly a decision taken by females, laying more eggs in the nest that will
be incubated by males. The simplest explanation for differences in clutch sizes
incubated by males and females might be the larger body size of males allowing them to
cover a greater number of eggs. However, this rarely seems to be a limiting factor of
clutch size in birds, particularly in galliforms (Lack 1947, Skutch 1982). Another
explanation could be that two females could be laying eggs on the same nest, a
behaviour relatively common in galliforms (Filchagov 1996; Storch & Segelbacher
2005), and confirmed in some nests of red-legged partridge by genetic analyses (Casas
et al. 2006b). However, this would imply a high frequency of poligyny that we have not
detected. Clutches incubated by males usually are the first laid by females (Green 1984,
Table 1), which may be more susceptible to nest parasitism due to longer exposure time,
although, again, this would imply a parasitism rate higher or more regular than the one
we have found (Casas et al. 2006a). Finally, given the low predation rate of clutches
incubated by males, females could be assigning more eggs to the clutch with higher
survival prospects, a strategy that could increase overall pair fitness.
Hatching Success
Infertility and death of embryos have been identified as the main cause of
hatching failure in captive red-legged partridges, accounting for a failure rate that may
be as high as 38 % of eggs (Cabezas-Díaz & Virgós 2007). From captive-breeding
studies, it is well known that the viability of red-legged partridge eggs before incubation
declines with exposure time, depending on environmental conditions (temperature and
48
Capítulo 1
humidity): long exposure periods before incubation, high temperatures, and low
humidity increase the probability of failure (Cancho 1992).
Clutches incubated by male partridges had poorer hatching success. Green
(1984) found a similar pattern in what he defined “delayed” and “undelayed” nests
(mostly male and female nests, respectively). Hatching success in nests of females can
be considered within the natural values for birds, about 90 % (Koenig 1982). However,
hatching failure in nests incubated by males was abnormally high, particularly late in
the season (20-90 % of eggs unhatched). Lower hatching success in male’s nests may be
explained by incubation capacity (Fernández & Reboreda 2007). There could be a limit
to clutch size imposed by brood patch size, because above a given threshold, birds could
not adequately warm all eggs, as suggested by several experimental studies with
artificially enlarged clutches (Monaghan & Nager 1997; Arnold 1999). Although body
size is usually not considered a limiting factor of clutch size in galliforms, this could
explain the negative relationship between clutch size and hatching success. An
alternative explanation may be that parasitic eggs appear more frequently in nests cared
by males (Casas et al. 2006a), and these eggs would have lower hatchability. However,
again parasitic eggs should be found at higher frequencies, and have a really low
hatching success to explain the large sex-related differences in hatching success we
have found. Finally, lower hatching success of nests incubated by males could be a
consequence of the longer period that eggs remain un-incubated in the male’s nests.
This would be consistent with the negative relationship between clutch size and
hatching success, given that larger clutches imply longer periods of exposure. Males do
not start incubating until females finish their second clutch, as reported by Green
(1984), and confirmed in our tabbed pairs. This might be a male’s strategy to increase
their paternity in second clutches. Late in the season temperatures are higher and
humidity lower, thus increasing the probability of hatching failure as breeding season
advances. This would suppose an additional constraint on the female’s decision to leave
a clutch under the care of his mate, that would be particularly astringent on years with
delayed laying: if laying starts late, a good deal of the investment devoted to eggs cared
by males could be lost.
49
Implications for the evolution of uni-parental care in birds
Phylogenetic analyses (Owens 2002), and experimental work with key species
(Kentish plover, Charadrius alexandrinus; Székely et al. 1999) suggest that population
density, and associated re-mating opportunities, is the critical factor behind the
appearance of female or male uni-parental care. When the benefits of deserting a clutch
are higher for females than for males, due to poor re-mating opportunities under
conditions of low population density, male-only parental care would appear. When the
opposite is true, female-only-parental care would be favoured. Red-legged partridge
populations may have a large variation in population density (Vargas et al. 2007), but
often around the threshold of density proposed by Owens (2002) as the limit between
species exhibiting male- or female-only parental care (1 nest every 10 Ha). We have
also found a high rate of divorce and re-mating within the same breeding season, as well
as cases of poligyny, EPPs, and intraspecific parasitism. Male care appears only under
good breeding conditions, while in poor years female-only care emerges. Red-legged
partridges could be in a situation near the female-only stage of parental care, in fact, a
common one in galliforms (Owens 2002), but depending on the environmental
conditions, male care would also be favoured. This system could be considered an
intermediate stage in the evolution of breeding systems, perhaps because typical
population densities of the species are often around the threshold suggested by
phylogenetic analysis. Further research on this species, particularly comparing the
occurrence and success of male brooding under similar environmental conditions, but
different population densities, may a be a critical work to advance within this line of
knowledge.
Management Implications
Although our partridge populations were subject to different game management

models, we failed to found differences in all the breeding patterns explored between
game estates (see also chapter 2). This lack of effect of game management could to be
due to several reasons. The simplest explanation is the lack of effect of hunting
management models on the breeding ecology of partridges, which might be much more
influenced by inter-annual variations in weather conditions and food availability. Our
results suggest that, according to breeding conditions, females lay eggs early or late in
50
Capítulo 1
the season, and that these different strategies could be an adaptation to climate
variations in mediterranean ecosystems (Blondel & Aronson 1999) and result from
strong interannual variations in food availability and/or predation risk (vegetation
growth and nest cover; Ricci 1985; Rands 1987; Ricci et al. 1990). In the studied game
estates, there was not food supply that could contribute to an improved body condition
during breeding season (Draycott et al. 2002). In other small game birds, this
management tool does not always increase clutch size or improve nesting success
(Hoodless et al. 1999), although it can help increasing densities of young birds
(Draycott et al. 2005). For red-legged partridge, additional food supply is a common
management tool, although, little is known about its effects on breeding performance. If
food availability is a limiting factor, it could be beneficial, but further research is needed
to explore the effects of food supplementation on breeding ecology.
ACKNOWLEDGEMENTS
We are very thankful to all game managers and hunting societies´ presidents
who kindly allowed us to work on their game estates, especially to Inocencio Bastante,
Lorenzo Sobrino, Delfín Martín de Lucía and Jose Juan Bermejo. Ambrosio Donate
provided invaluable data and multiple help. During this study F. Casas received support
from a pre-doctoral grant of the Junta de Comunidades de Castilla La Mancha (JCCM).
This work also received financial support from the research projects “Bases científicas
preliminares para un plan de conservación de la perdiz roja en Castilla-La Mancha” of
the Consejería de Agricultura y Medio Ambiente de la JCCM (Junta de Comunidades
de Castilla-La Mancha), and CYCIT projects MCYT-REN200307851/GLO and
CGL2004-02568/BOS. FM was supported by a NERC advanced fellowship, a Grant
from the Ministerio de Educación y Ciencia, Spain (CGL 2006-11823) and from the
JCCM, Spain (PAI06-0112).
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56
CAPÍTULO 2
Prácticas agrícolas o gestión cinegética: ¿Cuál es la clave para mejorar

el éxito reproductivo de la perdiz roja en las pseudoestepas agrarias?
Casas, F. & Viñuela, J. Agricultural practices or game management: which is the key to
improve red-legged partridge nesting success in agrarian pseudosteppes? Journal of Applied
Ecology, en evaluación.
Capítulo 2
ABSTRACT
1. Biodiversity of agrarian pseudosteppes is currently considered particularly

endangered in Europe. This kind of habitat holds important game species such as
red-legged partridges, which may add socio-economical and ecological value to
the ecosystem, and thus must be considered a priority species in management
programs integrating agriculture, hunting and conservation. We studied patterns
of partridge nesting habitat selection and nesting success to provide information
for the implementation of this kind of programs.
2. We evaluate nesting habitat selection of red-legged partridges (Alectoris rufa) in
“agrarian pseudosteppes”, their most widespread habitat where populations
reach highest densities. We present quantitative information on the factors
affecting nesting success, and the relative importance of predation versus other
causes of failure, and how these relate to nesting habitat.
3. Nests were found mainly in cereal fields, although this habitat was overall
negatively selected and had the lowest nesting success. Only lindes (herbaceous
strips among fields) were positively selected, and also was the habitat with
highest nesting success. Nesting habitat selection pattern showed stability among
years, hunting management methods and nesting periods. Nests within cereal
fields were mainly located close to the field margins (mostly < 5m), and
partridges selected positively this habitat only when considering the external
strip of the fields.
4. Agricultural practices, particularly harvesting, were the main cause of nest
failure, clearly more important than predation. In our case, this relatively low
importance of predation can not be due to the management related with predator
control. Changes in the agricultural system would be a more effective
management tool than predator control. In particular, maintenance and creation
of lindes and delay of harvesting in the most external strip of the cereal fields
would be the most efficient tools.
5. Synthesis and applications. The negative impact of harvesting on reproductive
success has been detected in other species typical of this habitat. Our results
show that a species with high socio-economic value, as the red-legged partridge,
also suffers the same problem, and this could give an easy way for collaboration
programs between hunters and conservationists. The information from this study
could be used to improve partridge breeding by managing agricultural areas, in
order to increase the availability of preferred nesting habitats (e.g. lindes). This
should be considered a priority among the eco-conditionality measures of the
new CAP, but unfortunately it has not been properly addressed by current
implementation of CAP in Spain.
INTRODUCTION
Agrarian pseudosteppes (open areas mainly aimed to dry farming) occupy a high
percentage of European surface, and are thus of vital importance for conservation of
European biodiversity (Pain & Pienkowski 1997). The advent of modern agrarian
management systems, agricultural intensification and land abandonment during the last
59
century, have modified the quality and quantity of available habitat, and consequently
the viability of many species (Chamberlain et al. 2000; Donald et al. 2001; Bota et al.
2005).
The red-legged partridge (Alectoris rufa) is a typical species of agrarian
pseudosteppes in southwestern Europe, where it has considerable socioeconomic value
in rural environments as a main game prey (Lucio 1998; Bernabeu 2000; Martínez et al.
2002). Yet, despite its importance as a quarry species, populations of this gamebird
have suffered marked declines during the last century throughout its range (Cramps &
Simmons 1980; Potts 1980), including Spain, the main stronghold of its worldwide
populations (Aebischer & Potts 1994; Blanco-Aguiar et al. 2004). Several reasons may
explain this decline, but the most important appears to be habitat alteration, particularly
the changes occurred during the last decades in agrarian management models (Lucio &
Purroy 1992, Blanco-Aguiar et al. 2004; Vargas et al. 2006, Blanco-Aguiar 2007).
Predation, overhunting, or problems associated with game releases, such as introduction
of new pathologies or genetic introgression, may also be of concern, at least locally
(Nadal 1992; Blanco-Aguiar 2007; Villanúa et al. In press), but little is known about the
relative importance of all of these factors. Blanco-Aguiar (2007) has recently concluded
that agricultural intensification, along with overhunting of declining populations, are the
main factors behind the deep decline in red-legged partridge hunting bags in Spain
during the last decades. However, little is known about which of the many disturbances
that agricultural changes have introduced in the ecosystems are behind the red-legged
partridge decline.
Ground vegetation height and cover around the nest have been described as the
main factors affecting nesting success of red-legged partridges (Rands 1988; Ricci et al.
1990). Nevertheless, most previous studies on red-legged partridge nesting habitat have
been limited to descriptions of habitat used (Potts 1980; Rands 1986; Rueda et al.
1993), whereas few studies have considered habitat selection (Rands 1988; Ricci et
al.1990). Moreover, these studies have been done on populations in the northern edge of
red-legged partridge range. In northern Europe, hedgerows and other permanent field
boundaries are considered important nesting habitats for this species. However, in the
Iberian Peninsula, these landscape structures are scarce, and field boundaries are formed
instead by strips of annual vegetation (“lindes”) in unploughed land. Intensification of
agriculture in Spain, as in other European countries, has been associated with a decrease
in the availability of this landscape feature (Pain & Pienkowski 1997; Fuller 2000).
60
Capítulo 2
Understanding nest habitat selection by red-legged partridge in the core of their

distribution area could generate potential tools for managers in developing strategies for
improving the availability of nesting habitat, including the maintenance and
development of field boundaries.
Additionally, the red-legged partridge, like other ground-nesting birds (Yanes &
Suárez 1995), is usually exposed to a high nest loss rate, and nesting success is thus a
very important parameter affecting population dynamics in this species (Potts 1980).
Previous studies showed that nesting habitat quality was a critical factor affecting
breeding success (Rands 1988; Ricci et al. 1990). Habitat management is thus
considered to be the main management strategy for the maintenance of sustainable wild
populations (Rands 1987a,b; Duarte & Vargas 2002). A positive correlation between
breeding density and the amount of suitable nesting cover has been found in this species
(Rands 1986). However, Reitz et al. (2002) found a high predation rate in preferred
nesting habitats. Thus, availability of favoured nesting habitat could affect breeding
density, but breeding success may be more influenced by other factors, such as
agricultural or game management.
Finally, the hunting community often considers predation as the main factor
behind reduced breeding success of this and other small game species in Spain (Nadal
& Comalrena 1994). This perception, along with recently increased legal protection of
many predators, and reduction in predator control permits issued (Nadal 1998) has led
to an increased legal or illegal control of predators, affecting negatively the populations
of endangered predator species (Viñuela & Villafuerte 2003). The scientific study of the
impact of predators on red-legged partridge breeding success has also received scarce
attention in Spain, but available information indicates that it may be highly variable
(reviewed by Yanes et al. 1998). The study of causes of nest loss in the most
widespread habitat of this species may help to clarify to what point predation is as
important as claimed by the hunting community, and this is a crucial piece of
information to start a solution to this conflict between game management and
biodiversity conservation (Valkama et al. 2005).
In this paper, we evaluate nest habitat selection for this territorial gamebird in its
most widespread habitat ecosystem, the “agrarian pseudosteppes”, where partridges
reach their highest densities (Blanco-Aguiar et al. 2003). We also present quantitative
information on the factors affecting nesting success, and the relative importance of
61
predation versus other causes of failure, and how these relate to nesting habitat. We
discuss our results in terms of management strategies for this important species.
Study area
The study area covered 125 km² and was located in Campo of Calatrava (Central
Spain, 38º 80´ N, 3º 80´ W, 610 m a.s.l.), within the city councils of Miguelturra and
Ciudad Real. This is an undulated farmland area dominated by a mosaic of crops,
mainly cereal (particularly barley), with interspersed patches of olive groves, vineyards,
and a few patches of dry annual legume crops (mainly vetch Vicia sativa) and sugar
beet Beta rubra. Natural vegetation areas are very scarce, including just some small
areas of short scrubland and pastureland mainly limited to the rocky top of hills. Other
crops, ploughed or abandoned farmland, and urban areas (mainly countryhouses) cover
less than 10% of the area.
Field work was developed within four game estates with marked different
hunting management models (see ESM). Predator control was the main management
tool applied in the study area, but with different intensity, according to the game estate.
Predator control of the most important partridge nest predators (corvids and canids, see
Herranz 2000, and Yanes et al. 1998), was mainly carried out over magpies Pica pica
(controlled through shooting and trapping), red fox Vulpes vulpes and feral or domestic
cats Felix catus and dogs Canis familiaris (controlled by shooting).
Data Collection
Partridge Captures and Monitoring
Fieldwork was carried out in spring and early summer from 2003 to 2005. Field
work was carried out on A, B and C hunting estates in 2003; A, B and D hunting estates
in 2004, and only in A and D hunting estates in 2005 (see chapter 4), due to policy
decisions by game estate managers about permission to work in their lands. Over the
three years, 115 adult partridges were captured in late winter/early spring (details in
62
Capítulo 2
ESM). We used cage traps with adult alive partridges inside as a decoy. Traps were
baited with wheat to additionally attract wild partridges. Each bird was fitted with a
necklace radio-transmitter with mortality sensor (BIOTRACK, 10 gr.), and released at
the capture site. After capture, we located birds every 1-5 days by radio-tracking, using
AOR-AR8200 multiband receptors and three element YAGI antennas. Sex was
determined in the field according to morphological traits (Sáenz de Buruaga et al.
2001), and subsequently confirmed by genetic analyses of blood samples (authors,
unpublished data).
Nest Location
The nests considered in this study were located using two methods. First, the
nests of ratio-tagged birds (n=47) were located by following the signal of tagged birds
showing a behaviour indicating that they were incubating (several consecutive days
located in the same point). Second, other nests (n=50) were found by systematically
searching suitable nesting habitat, defined as all substrates with enough vegetation
cover to install a nest. We based this selection on preliminary interviews with
gamekeepers, game managers and farmers, and on nesting site selection patterns
described in previous studies of this species. In subsequent years, we searched for nests
in habitats according to the pattern of nesting habitat selection found on the first year,
and some nests were also known by personal communications by farmers, gamekeepers
and shepherds. Both nest location methods (radio-tracking and systematic searching)
were used all study years (Table 3).
Nest Monitoring
Most nests (87%) were found once incubation had begun. The first time nests
were located, we recorded their exact position by GPS, date, type of habitat, and clutch
size. Nests were found in eight different habitat types (cereal, linde, fallow, vineyard,
country house gardens, scrubland, and leguminous crops and pastureland; detailed
description in ESM).
In subsequent visits (every 2 to 5 days), we recorded any variation in clutch size
(partial predation or additional eggs). Finally, we recorded the final fate of the clutch
(nest loss or success), the cause of nest loss when possible, and the date of failure or
63
hatching, which was determined according to clutch condition (broken, hatched or

disappeared). Also, once the final nest fate was known, and to avoid unnecessary
disturbance during incubation, we recorded data on the distance from the nest to the
nearest field boundary. Nesting success was considered to have taken place whenever at
least one chick had hatched (recognized by small regular breaks in the egg-shells, often
with one half of the shell within the other one, Bro et al. 2000b). Nest loss causes were
classified into six types: farming practices, predation, bad weather, desertion, cattle
trampling and unknown (detailed definitions in ESM).
The monitoring of “radio-tracking nests” was performed by radio-tracking
incubating birds at a distance of 1-5 m, approaching the nests only when adults were
away from the nest. The “no radio-tracking nests” were monitored by observation at a
distance of 1-2 m, also approaching the nests only when adults were not present.
The exact day when incubation started was known for 61 out of 97 nests. Other
nests were classified as “early” or “late” in relation to the mean start date of incubation
during the study period (17th of May, n=61). In each case, classification into one
category or other was made taking into account location date, number of days of
tracking, failure cause and state of the eggs prior to failure time. Whenever we had
doubts about when incubation started, or when the estimated date was around 17th May
(thus potentially falling into either category), we excluded data from these nests for the
analysis (n=7). All analyses were carried out exclusively with first clutches, excluding
replacement clutches (n=4).
Nesting habitat availability
We recorded the cover of each kind of habitat in each hunting estate monthly,
noting observations in maps where all parcels were marked, and subsequently calculated
the total surface of each habitat type using a GIS. For the analyses of nesting, we
calculated habitat availability during May, as the period when most nests were built (see
above). Habitat availability was measured as the proportional area of each habitat within
the study area. Using GIS, we also calculated (for cereal fields only), the surface
covered by the area between the edge of the field and 5 m inwards, between 5 and 10 m,
between 10 and 15 m and the remainder (further than 15 m from the edge). We selected
strips of 5 meters because we found the highest frequency of nests within this external
strip (see results), and also because it correspond to the width of combine harvesters
64
Capítulo 2
(and this could thus be the width that could be applied in management programs, such
as delay in harvesting of certain strips).
Statistical Analyses
Nesting habitat
To investigate the possible variation in the use of different nesting habitats

among the three study years, we performed a Chi-square analysis on a contingency table
with the variables habitat and year. Due to the low sample size for some habitats, we
pooled the data into four categories: cereal, linde, fallow and other (vineyards, country
house gardens, scrubland and leguminous crops). Similarly, we also explored possible
differences between sexes, nest location methods and nesting period (i.e., early or late)
in the nesting habitat used, using separate Chi-square analyses.
Given the importance of cereal fields as nesting habitat (see results), we
analyzed in more detail the nests located in this cover type, considering only those for
which precise data on the distance from the nest to the field boundary could be obtained
(n = 44). We tested for differences in field margin distance according to year and sex,
using a Generalized Linear Model (GLMz) with poisson error distribution and log link
function. If variation in field margin distance was explained by year, we conducted
pairwise comparisons.
Nesting habitat selection
Chi-squared goodness-of-fit analyses were used to compare observed values and

expected values according to the area occupied by each habitat (Byers et al. 1984).
Partridges nest in habitat with well developed vegetation, avoiding areas with low or no
cover. Therefore, we excluded from the analysis groves and ploughed fields. We
followed Bonferroni method to determine which habitats were positively selected or
avoided (Byers et al. 1984; see ESM).
Additionally, we also made a similar analysis, but dividing availability of “cereal
cover” in availability of the different parts of the cereal fields (peripheral strips as
described above).
65
Nesting fate
To analyze the factors that could affect nesting success we used a GLMz with
binomial error distribution and logit link function considering “success” as dependent
variable (success=1, unsuccessful=0), sex of the incubating bird (female red-legged
partridges may lay two clutches, one of them incubated by the male, Green 1984;
chapter 1), nest location method, nesting period, hunting management type, habitat
cover, year and their interactions as independent variables. A backward stepwise
procedure (Crawley 1993) was used to select the final model.
Secondly, a similar procedure was carried out for nests within cereal fields, with
field margin distance and year as independent variables.
Nest loss causes
To explore factors associated to different causes of nest loss, and due to the low
sample size for some of the nest loss causes, we pooled data into three categories:
predation, farming practices and other (unknown, bad weather, desertion and cattle
trampling). We employed a GLMz with multinomial error distribution and logit link
function, following a backward stepwise procedure (Crawley 1993), considering nest
loss causes as the dependent variable and sex, nest location method, nest period, hunting
management, habitat cover and year and their interactions as independent variables.
Additionally, for nests within cereal fields, we assessed the relationship between
distance to field margin and nest loss causes, using a similar procedure to that described
above.
All the analyses were performed with the statistical package STATISTICA 6.0.
RESULTS
Nesting habitat
Red-legged partridges nested in practically all habitats with vegetation cover

found in the study area, but with markedly different frequencies (Table 1, see ESM).
Although nests in cereal were more commonly located by radio tracking than by nest
searching, differences in habitat use in relation to nest location method were not
66
Capítulo 2
statistically significant (χ² = 6.61, df = 3; P = 0.09). We did not find significant

differences in the frequency of use of nesting habitats among years (χ² = 6.09, df = 6; P
= 0.41), between sexes (χ² = 4.24, df = 3; P = 0.24), or between nesting periods (χ² =
4.56, df = 3; P = 0.21).
Table 1. Red-legged Partridge nesting habitat use between 2003 and 2005 (n=97), compared with average
availability of each habitat type for the three years during May. Pattern of selection was estimated
following the method outlined by Byers et al. (1984), based on 95 % Bonferroni confidence intervals. See
ESM for a brief description of the methodology. In the second part of the Table we present an equivalent
analysis considering the availability of external strips in cereal fields and the location of nests within
those strips (n=44).
Habitat Expected Observed use 95% Preference*

use (pei)¹ (poi)² limits
Cereal 0.634 0.474 0.336- -
0.613
Fallow 0.045 0.124 0.032- 0
0.215
Pastureland 0.056 0.031 0-0.079 0
Linde 0.002 0.227 0.111- +
0.343
Vineyards 0.053 0.072 0-0.144 0
Country house gardens 0.031 0.031 0-0.079 0
Scrubland 0.158 0.031 0-0.079 -
Leguminous crops 0.022 0.010 0-0.038 0
Distance to field boundary
(m.)
0 to 5 0.127 0.591 0.412- +
0.77
5 to 10 0.118 0.136 0.011- 0
0.261
10 to 15 0.109 0.045 0-0.121 0
>15 0.645 0.227 0.075- -
0.384
¹The relative area of the habitat.
²Calculated for habitat i as poi = ni/N, where ni is the number of nest of red-legged partridge were located in that habitat and N is the
total number of observations across all habitats.
*Preference: +, use significantly greater than expected; -, use significantly less than expected; 0, use no different to expected.
A high percentage of the nests in cereal fields (72.7%) were located within 10 m
from the field margin, mostly (59.1 %) within the first five meters (see ESM). The
average distance to the edge of the field in nests within cereal did not vary significantly
between sexes (χ² = 0.67, df = 1; P = 0.41), but varied significantly among years (χ² =
9,72, df = 2, P < 0.01). Field margin distance was lower in 2004 (4,69 ± 6,04 m) than in
67
2003 (17,94 ± 5,88 m; χ² = 6.95, df = 1; P < 0.01), or in 2005 (31,99 ± 9,68 m; χ² =

11.76, df = 1; P < 0.001). No significant differences were found between 2003 and 2005
(χ² = 0.91, df = 1; P = 0.34).
Nesting habitat selection
The pattern of nesting habitat use by partridges differed significantly from that
expected from the area occupied by each habitat in the study area (χ² = 2657.003, df =
7; P < 0.001). Bonferroni analysis indicated that partridges positively selected lindes,
and negatively scrubland and cereal fields. No positive or negative selection was
detected for other habitat types (Table 1).
When considering availability of cereal in relation to the distance to the field
edges, the most external strip (0 to 5 m from the edge) was positively selected, while the
area at distance further than 15 m from the field margins was negatively selected (χ² =
87.94, df = 3; P < 0.001; Table 1).
70
60
50
% Success
40
Early Nest
Late Nest
30
20
10
0
2003 2004 2005
Year
Figure 1. Percentage of red-legged partridge nests those were successful in relation to year and breeding
period.
Factors affecting nesting failure
Overall rate of nest loss in the red-legged partridge in our study area was
relatively high (63.92 % of 97 nests). Success was higher in “early nests” than in “late
nests” (all years combined), although differences between periods varied among years
68
Capítulo 2
(significant Year*“Nesting Period” interaction; Table 2), because the trend was reversed
in 2004 (Fig. 1). Nests incubated by males had higher success probability (0.77) than
those incubated by females (0.43; Table 2). Finally, we also found significant variation
in nesting success in relation to nesting habitat, nests located in lindes having the
highest success, whereas nests within cereal fields had the lowest (Fig. 2). Other
variables had no significant effect on nesting success (Table 2).
Table 2. Results of the model analysing factors affecting nesting success (dependent variable) of red-
legged partridges in our study area (GLMz procedure).
Source of variation d.f. wald P

Year 2 0.308 0.857
Hunting Management 2 3.920 0.141
Location Method 1 1.011 0.315
Sex 1 13.019 0.0015
Nesting habitat 3 10.754 0.013
Nesting Period 1 5.338 0.021
Year x Nesting Period 2 8.100 0.017
For nests in cereals fields, we did not find significant differences in nesting
success related to distance to field margin (Wald = 0.08; P = 0.77) or among years
(Wald = 3.54; P = 0.17).
0.70
0.60
0.50
% Success
0.40
0.30
0.20
0.10
0.00
Cereal Fallow Linde Other
Nest Habitat
Figure 2. Nesting success (mean ± 95% confidence intervals) in relation to nesting habitat for the red-
legged partridge in central Spain, 2003-2005.
69
Nest loss causes
The main cause of nest loss was farming practices (ploughing and particularly
harvesting) affecting to 56.4 % of all failed nests (Fig. 2), a percentage almost three
times higher than the proportion of nests lost to predation (20.97 %). Causes of failure
did not significantly vary among years (Fig. 3), hunting management models, nest
location methods or nesting periods (Table 3). We found significant differences in nest
loss causes related to sex of the incubating bird and nesting habitat (Table 3). Nests
incubated by females were more affected by farming practices, as were nests placed in
cereal fields.
For nests in cereal fields, we did not found differences in nest lost causes in
relation to field margin distance (Wald = 1.15; P = 0.76).
Table 3. Factors affecting nest lost causes (dependent variable) of red-ledged partridges in our study area
(GLMz Multinomial procedure).
Source of variation d.f. wald P

Year 2 0.361 0.645
Hunting Management 2 1.215 0.304
Location Method 1 0.0027 0.958
Sex 1 56.578 < 0.05
Nesting habitat 3 1.173 < 0.001
Nesting Period 1 0.732 0.4135
DISCUSSION
In a landscape dominated by agricultural land we found that red-legged partridge

nests were mainly located in cultivated substrata, which contrasts with other studies,
where hedgerows and natural vegetation were the main nesting habitat (Rueda et al.
1993; Ricci et al. 1990; Green 1984; Rands 1987a). Both in our study and previous
studies (Rands 1986; Rands 1988; Ricci et al. 1990), red-legged partridges selected
positively linear landscape features for nesting, and negatively cereal fields. This is in
agreement with the habitat selection pattern of adult birds during breeding season
(Fortuna 2002). Fallows could potentially be an important nesting habitat, but due to
agricultural intensification they are an increasingly scarcer habitat in agricultural areas
(Pain & Pienkowski 1997). Perhaps as a consequence of their scarcity and dispersed
occurrence, we did not find that fallows and natural vegetation were positively selected
by partridges in our study area. Lindes occupied only 0.19 % of the area, and although
they were the most preferred habitat they were not the one containing more nests. On
70
Capítulo 2
the other hand, well vegetated lindes are also relatively scarce in our study area, and this
may be forcing partridges to use negatively selected agricultural substrata, rarely used in
other areas. Because nesting habitat influenced nesting success, in this species as in
other galliforms (Taylor et al. 1999; Tirpak et al. 2006), cereal fields could be
considered a suboptimal unselected habitat working as an ecological trap (Battin 2004).
50
Success
45 Lost due to predation
Lost due to farming practices
40
Lost due to unknown causes
35
30
25
20
15
10
5
0
2003 2004 2005
Figure 3. Final nest fate of red-legged partridge nests in the study area during the study period (n=62).
Percentage of nests, data pooled for 2003-2005.
As previously reported (Ricci et al. 1990; Bro et al. 2000a), nests in cereal fields
were mainly located close to the field margins, and partridges positively selected the
most external strip (0 to 5 m from the edge) of the cereal fields, further supporting the
importance of field boundaries. Partridges nesting close to the edge in cereal fields may
benefit from increased food abundance in field boundaries (Thomas & Marshall 1999),
but they may also suffer from increased predation risk in linear habitats (Haensly et al.
1987; Ricci et al. 1990). However, we did not find significant differences in nesting
success in relation to distance to field boundaries, and lindes were the most successful
nesting habitat, both results contradicting that predation may be a problem for nests in
this habitat.
Agricultural practices, particularly harvesting, were the main cause of nest
failure in red-legged partridge, clearly more important than predation. Differences
among years in the pattern of nesting success with respect to nesting period, 2004
showing higher failure rate for early nests, may be due to differences in agricultural
71
management among years, a result highlighting the importance of this factor to improve
nesting success of this species. In 2004, early harvesting of green cereals for livestock
food was particularly frequent (pers. obs.). The high rate of nest loss caused by
agricultural practices may be the consequence of the pattern of nest location in the study
area. Other studies have also pointed out the strong impact of agricultural practices on
nesting success of this species (see Potts 1980 and Vargas & Cardo 1996). Additionally,
it is important to highlight that the study area is a good example of the typical
agricultural landscape prevailing in the range of red-legged partridges in Spain, where
their populations reach maximum densities (Vargas et al. 2006), and therefore, the
strong negative effect of agricultural practices we are reporting may also affect partridge
populations in wider areas. Thus, perhaps it might be considered the main factor with
negative effect in red-legged partridge reproduction even at a national scale, supporting
the results of long-term hunting bag analyses showing that agricultural change may
have been the main factor behind red-legged partridge declines in Spain (Blanco-Aguiar
2007).
The relatively low importance of predation in our study can not be due to the
management related with predator control. In fact, there were large differences among
study areas in relation to the intensity of predator control, but no significant differences
in nesting success and nest loss causes among hunting management schemes were
found. Besides, one of the hunting management models was characterised by non-
intensive predator control (see ESM). Main predators of partridge nests (Herranz 2000),
which are generalist predators associated to human activities and buildings, were
common in our study area, near two large villages and holding a large number of
dispersed countryhouses. Predator control is the game management tool more
widespread in Spain (Arroyo & Beja 2002), but our results show that, at least during the
incubation period, changes in the agricultural system would be a more effective
management tool than predator control.
Management implications
As in other studies (Rands 1987a; Bro et al. 2000b), our results showed the
crucial importance of lindes as a nesting habitat, since it was the nesting substrate with
highest breeding success, and was strongly selected as nesting site too. Several studies
have shown that highest red-legged partridge densities are found in areas with higher
72
Capítulo 2
fragmentation and hedge abundance (Rands 1986; Peiró 1992; Lucio & Purroy 1992;
Blanco-Aguiar et al. 2003). However, up to now, no clear proximate reasons had been
presented to explain this general pattern. Our results suggest that the high nesting
success associated with nests located in lindes can be a key factor explaining higher
partridge abundance in landscapes with abundant and well preserved lindes, while low
success in cereal fields would explain low abundance on areas with large agricultural
exploitations. Again, the main conclusion for partridge managers, something already
practiced by some "select managers”, which follow their own personal experience, is
that the key to improve red-legged partridge productivity are actions on agricultural
management.
In that sense, slight delays in cereal harvesting could be an important tool to
improve red-legged partridge reproductive success. More specifically, stopping or
delaying harvesting in a strip of 5 m surrounding the cereal fields might be an effective
partridge management action. The difference found in nesting success between sexes
could be due to differences in incubation onset (Green 1984). This result also illustrates
how small differences in hatching dates or in harvesting dates, could be very important
for reproductive success of this species, intimately tied to the agricultural cycle. It is
interesting to outline that these actions could also be favourable for other species using
similar nesting habitat (cereal fields), such as little bustards (pers. obs.), great bustards
(Morgado & Moreira 2000), or Montagu´s harrier (Ferrero 1995). The negative impact
of harvesting on reproductive success has been observed in the Montagu´s harrier
(Castaño 1995, Arroyo et al. 2002) or the little bustard (Carole Attié, Personal
Communication). Our results show that a species with high socio-economic value, such
as the red-legged partridge, also suffers from the same problem and this could give
course for collaboration programs between hunters and conservationists.
In the Spanish “pseudosteppes” there are the largest numbers of steppe bird
species in the EU (Tucker 1991), most of which are Species of European Conservation
Concern (SPECs). Indeed, the pseudosteppes contain one of the greatest proportions of
regularly occurring species that are SPECs (Tucker & Heath 1994). Our study area is a
typical example of the agricultural landscape that prevails in the distribution range of
red-legged partridges, at least in Spain. This means that the information from this study
could be used to improve partridge breeding by managing agricultural areas, in order to
increase the availability of preferred nesting habitats. Maintaining or increasing lindes
in agricultural areas along with cereal harvesting management would have a positive
73
effect on partridges and elsewhere in Spanish farmland (Tella et al. 1998; Vickery et al.
2002), and should be considered a priority among the eco-condicionality measures of
the new CAP. Providing financial incentives to farmers that voluntary address these
concerns could also play an important role in reproductive success. Unfortunately,
current implementation of eco-conditionality measures of CAP in Spain have not
properly incorporated management of lindes as a priority (BOE 2004).
ACKNOWLEDGMENTS
Salvador Luna, Gustau Calabuig, Antonio Linares, Jesús Martínez-Padilla,

Laura Iglesias, Fabián Casas Castellanos, Carlos and Jesús Nieto Arenas helped with
field work. Fidel Sanchez-Campos helped with GIS and habitat availability data. We are
also thankful to all game managers and hunting societies´ presidents who kindly
allowed us to work on their game estates, especially to Inocencio Bastante, Lorenzo
Sobrino, Delfín Martín de Lucía and Jose Juan Bermejo. Ambrosio Donate provided
invaluable and multiple help. We thank Beatriz Arroyo, Steve Redpath, Raimundo Real,
Javier Bustamante and an anonymous referee for their helpful comments of earlier
drafts of the manuscript. During this study FC received support from a pre-doctoral
grant of the Junta de Comunidades de Castilla-La Mancha (JCCM) and financial
support from the CYCIT projects MCYT-REN200307851/GLO and CGL2004-
02568/BOS.
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differently vegetated margins of arable fields. Agriculture, Ecosystems and
Environment 72, 131-144.
Tirpak, J.M., Giuliano, W.M., Miller, C.A., Allen, T.J., Bittner, S., Edwards, J.W.,
Fridhof, S., Igo, W.K., Stauffer, D.F. & Norman, G.W. (2006) Ruffed grouse
nest success habitat selection in the Central and Southern Applachians. Journal
of Wildlife management 70, 138-144.
Tucker, G. (1991) The status of lowland dry grassland birds in Europe. (eds. Goriup,
P.D.L., Batten, A. & Norton, J.A.), pp. 37-48. The conservation of lowland dry
grassland birds in Europe. Peterborough: Joint Nature Conservation Committee.
Tucker, G.M & Heath, M.F. (1994) Birds in Europe: their conservation status. Birdlife
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Reviews 80, 171-203.
Vargas, J.M. & Cardo, M. (1996) El declive de la perdiz roja en el olivar. Trofeo 317,
23-27.
yields in southern Spain. European Journal of Wildlife Research 52, 188–195.
Vickery, J., Carter, N. & Fuller, R.J. (2002) The potential value of managed cereal field
margins as foraging habitats for farmland birds in the UK. Agriculture,
Ecosystem & Environment 89, 41-52.
Gortázar, C. (In press) Sanitary risks of red-legged partridge releases:
10.1007/s10344-007-0130-2.
Viñuela, J. & Villafuerte, R. (2003) Predators and rabbits in Spain: a key conflict for
European raptor conservation. (eds. D.B.M. Thompson, S. Redpath, A. Fielding,
M. Marquiss & C.A. Galbraith), pp. 511-526. Birds of prey in a changing
environment. The Stationary Office, London, UK.
78
Capítulo 2
Yanes, M. & Suárez F. (1995) Nest predation patterns in ground-nesting passerines on

the Iberian Peninsula. Ecography 18, 423-428.
Yanes, M., Herranz, J., de la Puente, J. & Suárez, F. (1998) La Perdiz Roja. Identidad
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Madrid.
79
ELECTRONIC SUPPLEMENTARY MATERIAL (ESM)
DESCRIPTION OF HABITAT TYPES FOUND TO BE NESTING HABITAT OF

RED-LEGGED PARTRIDGES
Cereal: barley, wheat, hard wheat, oats, rye and cereal mix.
Linde: linear annual vegetation patches in strips of unploughed land placed between
cultivated plots or between the plots and tracks.
Fallow: unploughed fields with herbaceous annual vegetation that had been cultivated in
previous years.
Pastureland: natural low herbaceous vegetation.
Vineyard: traditional or modern cultivation system with guiding wires.
Country house gardens: nests found just in the external hedge or inside country house
fenced gardens.
Scrubland: Mediterranean short scrubland in small patches.
Leguminous crops: peas Pisum sativum and vetch.
DEFINITION OF THE CAUSES OF NEST LOSS
Farming practices: vegetation cover was mowed or harvested, eggs were broken and
compressed into the nest or the adult partridge had not come back to the nest after
harvesting.
Predation: when large fragments of shell were found scattered around the nest or eggs
had disappeared.
Weather: whenever failure occurred just after a strong storm.
Desertion: eggs were found cold, after birds had disappeared for at least one day.
Cattle trampling: if there were cattle foraging inside the nest field and the eggs were
found crushed.
Unknown: when we could not clearly assign failure to any of the previous causes.
BONFERRONI METHOD (Byers et al. 1984)
It is based on the calculation of simultaneous confidence intervals for the true

proportion of utilization for each habitat, applying the formula in Byers et al. (1984)
with a Z0,003125= 2.734369. Once the so-called 95 % “bonferroni intervals” of
confidence were calculated. Lastly, we checked if the value of “expected use” was
inside the interval (no selection), over the interval (positive selection) or under interval
(negative selection).
80
Capítulo 2
Table 1. Main traits of the hunting management models in the four game states, inside the study area.
Data in first column provided for states A and C respectively.
Hunting management Model 1 (A and C) Model 2 (B) Model 3 (D)

traits
Surface covered (Ha) 3145 and 1009 1484 548
Kind of Exploitation Extensive Intensive Extensive
Nº of hunters High High Low
Hunting bag Variable among years, High hunting bags, the same Different among years,
(average study period hunting pressure adjusted to hunting pressure all years hunting pressure adjusted to
birds/year/hectare) autumn populations (0,26 and (1,35 birds/year/hectare) autumn populations (0,55
0,15 birds/year/hectare) birds/year/hectare)
Predator control Only during late breeding During all year During all year
season
Artificial water points Yes Yes Yes
Artificial food points No Yes Yes
Refuges No Yes No
Releases of farm-bred No Yes No
partridges
Hunting of rabbits No Yes Yes
Controlled rabbit - No (about 2000 rabbit/year) Yes (about 500 rabbit/year)
hunting bags
Table 2. Red-legged Partridges captured and radio-tagged during the study period, classified by hunting
state, year and sex.
Hunting state Total
Year A B C D ♂ ♀
2003 7♂/3♀ 9 ♂ / 11♀ 5♂/4♀ 21 18
2004 10 ♂ / 6 ♀ 7♂/8♀ 5♂/8♀ 22 22
2005 5 ♂ / 11 ♀ 7♂/9♀ 12 20
Total 22 ♂ / 20 ♀ 16 ♂ / 19 ♀ 5♂/4♀ 12 ♂ / 17 ♀ 55 60
Table 3. Red-legged partridge nests found in the three study years, classified by location method (see
methods for details).
Location Method 2003 2004 2005 Total

Radiotagged birds 23 13 11 47
Untagged birds 15 25 10 50
Total 38 38 21 97
81
80
70
Use
60 Availability
50
Average %
40
30
20
10
e
w
l
ps
ns
ea
rd
nd
an
n
l lo
la
o
e
er
ya
Li
Fa
bl
cr
rd
re
C
ne
ru
ga
us
u
st
Sc
Vi
o
e
Pa
in
us
m
ho
gu
ry
Le
nt
ou
C
Figure 1. Used vs available nesting habitat for red-legged partridge in the study area. Availability is
referred to the whole area analysed, excluding non-vegetated habitat, and used is referred to the total
number of nests analysed (n=97). Data pooled for 2003-2005.
70
60
50
Frecuency (%)
40
30
20
10
0
<5 <10 <15 <20 <25 <30 <35 >35
Distance to field boundary (m)
Figure 2. Frequency distribution of distance to the field boundary for red-legged partridge nests within
cereal fields (n=44). Data pooled for 2003-2005.
82
CAPÍTULO 3
Consecuencias fenotípicas y sobre la eficacia biológica de la

introgresión genética en poblaciones silvestres de perdiz roja Alectoris
rufa
Casas, F., Sánchez-Barbudo, I., Mougeot, F., Dávila, J.A. & Viñuela, J. Phenotypic and fitness
consequences of genetic introgression in wild red-legged partridges Alectoris rufa. En
preparación
Capítulo 3
ABSTRACT
1. Hybridization is a widespread phenomenon, which in natural conditions plays

crucial roles in the speciation and diversification of animals. Hybridization may
also be artificially produced by crossing two allopatric species in captive
breeding. Unnatural mixing of historically isolated taxa due to human-related
activities has increased in recent decades, favouring levels of hybridization and
introgression that can have drastic ecological implications whenever these
animals are introduced into wild populations.
2. The red-legged partridge (Alectoris rufa) is currently the most important
gamebird in Spain, with a high socioeconomic value in rural environments.
Given the declines experienced by wild partridge populations over last decades,
the releases of farm-reared partridge have become a generalized management
strategy (at least 3-4 million birds released every year). Anthropogenic
hybridization in captivity with chukar partridge (A. chukar), aimed at increasing
the productivity of farmed birds, and game releases have extended the problem
into the wild.
3. Our main aims were to quantify the occurrence of hybrids in a natural
population located in central Spain and to investigate fitness differences between
hybrid and non-hybrid wild red-legged partridges. We used a wide range of
phenotypic and fitness indicators (body size, body condition, physiology,
reproductive performance, survival and mortality causes) to evaluate the
consequences of genetic introgression in a wild red-legged partridge population.
4. We found introgression with A. chukar genes in 28.7 % of wild red-legged
partridges. The proportion of hybrids did not differ significantly between sexes
or between years, but differed between game estates. The occurrence of
partridges with allochtonous lineages was higher in a game estate where releases
occurred in the last 8 years than in game estates where no releases were
performed in the last 15 years. Hybrids were smaller than non-hybrid birds, only
in males. Body condition did not differ between hybrid and non-hybrid males,
but hybrid females were in better body condition than non-hybrid ones. Hybrid
females, but not males, had significantly lower plasma carotenoid
concentrations, which may limit their use of carotenoid pigments for ornamental
coloration, self maintenance or allocation to eggs.
5. In males, incubation probability differed between years, and tended to be higher
for hybrids than for non-hybrids, whereas no differences were found in females.
Laying dates did not differ significantly between hybrid and non-hybrid females.
However, hybrid females laid larger clutches than non-hybrid ones. Variation in
hatching success was not explained by genotype. Hybrid birds had lower
survival rate than non-hybrid ones and this difference was mainly due to higher
predation rates on hybrid birds.
6. Synthesis and applications. Overall, our results confirm a serious risk of genetic
contamination of partridge populations due to game releases of farm-bred birds.
The situation may be impaired by good breeding performance of hybrid females
in the wild. Thus, controlling the introgression of allochthonous genomes is a
piece of vital importance for the long-term conservation of this species. Urgent
management programs aimed at stopping releases of hybrid birds, renewing
genetic pools in areas with genetic introgression, and preserving areas with
populations in good genetic conditions are urgently needed to preserve this
species as such.
85
INTRODUCTION
Understanding the genetic basis of fitness in natural populations has long been a
central aim in ecology and evolution. Hybridization is a widespread phenomenon
(Rhymer & Simberloff 1996; Avise 2004), and in natural conditions, it plays crucial
roles in the speciation and diversification of animals (Rhymer & Simberloff 1996;
Avise 2004; Barton 2001). Hybridization may cause either decreased fitness
("outbreeding depression") or increased fitness ("hybrid vigor"). Outbreeding
depression is a fitness reduction seen in hybrid individuals suffering from
underdominance (heterozigosity disadvantage), and/or the disruption of beneficial
interactions (e.g. between genes and the environment) or intrinsically coadapted gene
complexes (Templeton 1986; Frankham 1999). However, hybridization can also create
beneficial gene interactions, including overdominance (heterozygote advantage) and
dominance (the masking of deleterious effects), leading to hybrid vigor. In many taxa,
relatively heterozygous individuals are often fitter than homozygous individuals (Keller
& Waller 2002).
Because of its potential effects on individual fitness (Allendorf et al. 2001;
Keller & Waller 2002), hybridization is also important to conservation biology. In birds,
natural hybridization is more common between parapatric species than between
sympatric species pairs, either because species recognition mechanisms may be
underdeveloped in parapatric species or because of restriction mechanisms of mate
choice in contact zones (Mayr 1942; Randler 2002). Unnatural mixing of historically
isolated taxa due to human-related activities has increased in recent decades, favoring
levels of hybridization and introgression that can have drastic ecological implications
(Olden et al. 2005; Randi 2008). Hybridization could thus to be a threat to natural
populations, especially when it occurs as a consequence of human activities, due to the
introduction of new species or habitat fragmentation or modification (Rhymer &
Simberloff 1996). Thus, it is important to separate the evolutionary role of natural
hybridization from problems associated with increasing anthropogenic hybridization
(Allendorf et al. 2001). Among these human-induced cases of hybridization in the wild,
the massive releases of gamebirds for hunting purposes may be a particularly
widespread and worrying factor, which only recently has received the necessary
attention (Randi 2008).
86
Capítulo 3
Natural hybridization may occur sporadically between broadly sympatric species

or be confined to particular contact areas (Avise 2004). The formation of hybrid zones
can be promoted by biological or human-induced invasions, if introduced species are
close enough to native species. Natural hybridation zones have been described in
several locations for partridge species of the genus Alectoris (Barilani et al. 2007). In
the southern French Alps and Italy, red-legged partridge (Alectoris rufa) interbreed with
rock partridge (A. graeca), with hybrids being viable and fertile (Bernard-Laurent 1990;
Randi & Bernard-Laurent 1998, 1999;). In the Iberian Peninsula, the red-legged
partridge and the barbary partridge (A. barbara) are both present on the Rock of
Gibraltar, where the later was introduced at the last of the nineteen century (Lorenzo &
Martí 2003), but no cases of hybridization have been described between these two
partridges species. Hybrids between red-legged partridges and chukar partridges (A.
chukar) have been found in an introduced population in Italy (Baratti et al. 2004;
Barbanera et al. 2005), on the Island of Majorca (Tejedor et al. 2007) and are
widespread in the Iberian Peninsula, especially in areas where farm-bred partridges are
released for hunting purposes (Blanco-Aguiar 2007). Genetic introgression in
continental Spain seems to be a general pattern of human origin, due to higher
productivity in farms of chukar partridges or their hybrids with red-legged partridges
(Nadal 1992), and the lack of control of the genetic quality of farm-bred partridges
(Blanco-Aguiar 2007). Partridges with allochthonous lineages have been more
commonly found in game estates where farm-reared partridge releases took place
(Blanco-Aguiar 2007). Anthropogenic hybridization in captivity aims at increasing the
productivity of farmed birds, and game releases have extended the problem into the
wild.
The red-legged partridge is actually the most important game bird in Spain,
especially in farmland areas, and has a high socioeconomic value in rural environments
(Lucio 1998; Bernabeu 2000; Martínez et al. 2002). However, this small gamebird is
currently considered as a “vulnerable” species, due to widespread declines in wild
populations and increasing genetic introgression with allochtonous partridges
(Aebischer & Potts 1994). Given the problems experienced by wild partridge
populations, many game managers have been releasing large numbers of birds over the
last 30 years in Spain (at least 3-4 millions every year; Garrido 2002). This contributes
to a profitable business of captive breeding and rearing of partridges in farms, which has
increased exponentially since the 80´s, and has made of restocking one of the main
87
management tools currently used in Spain. As a result, hunting bags of partridges in

recent years have recovered to reach between 3 and 4.5 million partridges hunted per
year (Garrido 2002). However, this management system does not appear to help the
recovery of wild partridge populations (Gortázar et al. 2000; Pérez et al. 2004; Blanco-
Aguiar 2007) that appear to benefit more from other management techniques,
particularly habitat management (Rands 1987a, b; Duarte & Vargas 2002; chapter 2).
Moreover, problems associated with game releases, such as introduction of new
pathologies, may also be of concern, at least locally (Nadal 1992; Millán et al 2004;
Villanúa et al. In press). Albeit the widespread hybridization of red-legged partridges in
Spain and its potential as serious problem for the conservation of the species, as well as
the socio-economic importance of this gamebird, virtually nothing is know about the
fitness of hybrid birds in natural populations, and thus the potential impacts that releases
of captive bred birds may have on these populations. However, this information is
particularly important, because depending on the relative importance of outbreeding
depression or hybrid vigor, introgressed partridges would extend more or less rapidly
within wild populations. It is well known that released partridges in general have low
survival after release in the wild (Gortázar et al. 2000), but it is also known that released
farm-bred partridges are able to establish in the wild and breed successfully (Duarte &
Vargas 2004), and that hybrid birds are commonly found in the wild.
Here, we investigate phenotypic and fitness differences between hybrid and non-
hybrid wild red-legged partridges in central Spain over three years. We used a wide
range of phenotypic and fitness indicators to evaluate the consequences of genetic
introgression in a natural red-legged partridge population located in central Spain. As
phenotypic indicators of fitness, we looked at body size, condition and plasma
carotenoid levels. Body size might be important in a competitive context, in particular
in intra-sexual competition between males for access to territories and mates, and
between females for access to mates. Because males are larger than females, and
because chukar partridges are larger than red-legged partridges (Cramps & Simmons
1980), size might differ between introgressed and non-introgressed red-legged
partridges, depending on the sexes. Because hybrid birds might have different
vulnerability to diseases or predators, they might also have different health, condition,
and survival rates than “pure” red-legged partridges. As indicators of health and
condition, we looked at body mass corrected for size and plasma carotenoid levels.
Carotenoid pigments are used by partridges either for ornamental coloration (Pérez-
88
Capítulo 3
Rodríguez 2007), for self maintenance (parasite resistance and immune response; Blas
et al. 2006) or for reproduction (females allocate carotenoid to eggs) (Bortolotti et al.
2003). Vertebrates cannot synthesize carotenoids de novo, but must ingest them, so diet
may limit ornament expression and good foragers, in better condition, are expected to
acquire more carotenoids (Olson & Owens 1998; Hill & McGraw 2006). In addition,
carotenoids act as immune-enhancers and are beneficial for health and self maintenance
(Olson and Owens 1998; Moller et al. 2000), and are currently considered as signals of
individual quality (Pérez-Rodríguez et al. in press). Birds with more parasites are
expected to have lower carotenoid levels than healthier birds (e.g. Mougeot et al. 2007).
Differences in condition and carotenoid levels between hybrid and pure partridges
would thus be indicative of differences in foraging ability and health. We also measured
the survival and breeding performance of hybrid and non-hybrid birds. We expected
hybrid birds to survive less well that “pure” wild partridges, and in particular to be more
vulnerable to predation. Farm-reared birds are often selected to maximize breeding
outputs, but is also known that inbreeding depression may exist in this species
(Woodard et al. 1982), and that could be a common phenomenon in small-size,
domestic farms with poor management system, not rarely found in Spain. Thus,
introgressed red-legged partridges might have higher or lower breeding success and
survival rate than non-hybrids ones.
Study area
We conducted the study in central Spain, on a 125 km² area located in Campo of
Calatrava, Ciudad Real (38º 80´ N, 3º 80´ W, 610 m a.s.l.). The study area was mainly
agricultural, dominated by a mosaic of crops (mainly cereal), with interspersed patches
of olive groves, vineyards, and a few patches of dry annual legume crops (mainly vetch
Vicia sativa) and sugar beet Beta rubra. Natural vegetation areas are very scarce,
including just some small areas of short scrubland and pastureland mainly limited to the
rocky top of hills. Other crops, ploughed or abandoned farmland, and urban areas
(mainly countryhouses) cover less than 10% of the area. Because harvesting (shooting)
of red-legged partridge occurred on the study area, some management was conducted
for hunting purposes. Management included mainly predator control, provision of
89
drinking stations, and the release of captive bred birds (see chapter 2 for more
information). Predator control targeted mostly magpies Pica pica (controlled through
shooting and trapping), red foxes Vulpes vulpes, feral cats Felix catus and feral dogs
Canis familiaris (controlled by night shooting).
Captures and measurements
Fieldwork was carried out in February-October 2003-2005. A total of 115 adult

partridges were captured in February-May (2003: n = 39, 2004: n = 44, 2005: n = 32;
see chapter 4), using cage traps baited with wheat and with an alive partridge inside the
cages as a decoy. All captured birds were individually ringed and sexed from plumage,
morphology and ornaments (Sáenz de Buruaga et al. 2001). Sexing was subsequently
confirmed by genetic analyses using blood samples (authors, unpublished data). For
each bird, we recorded capture date (julian date; 1 = 1st of January) and measured the
following: (1) body mass, with a 1000g Pesola® precision scale; (2) tarsus length, (3)
beak length and (4) head width, with a digital calliper to the nearest 0.01 mm; (5) tail
length, (6) total body length, and (7) wing length, with a ruler to the nearest 0.5 mm. All
measurements were taken according to Svensson (1992) and by the same person (FC).
We also took a blood sample from the brachial vein (0.5-1 ml) using a
heparinized syringe, and fitted each bird with a 10g necklace radio-transmitter with a
mortality sensor (BIOTRACK, 10 gr.). All birds were released at the site of capture and
monitored by radio-tracking using AOR-AR8200 multiband receptors and three element
YAGI antennas.
Breeding performance and survival
We located and monitored partridges using radio-tracking 2-4 times every week
from capture until October, before hunting season started.
For each female we recorded whether it laid and incubated a clutch (1
=incubation, 0 = no incubation), the day incubation began (julian date; 1 = 1st of April),
clutch size, hatching success (1= clutch successfully hatched > 1chick; 0 = failed to
hatch), and breeding success (number of young fledged / clutch size). Double-brooding
occurs frequently in red-legged partridges (Green 1981, 1984; chapter 1). Females
often lay in two nests, one incubated by the female, the other one by the male. For
90
Capítulo 3
females, we tested for differences between hybrids and non-hybrids in incubation

probability, laying date, clutch size and hatching success. For males, we tested for
differences between hybrids and non-hybrids in incubation probability and hatching
success, but not laying date or clutch size, because we did not know the genetics of the
female which laid the clutch. Some individuals died before breeding (n =18 females, n
=15 males) so sample size was reduced for the analyses of breeding performance.
For survival analyses, we used data collected over three years on 89 adult red-
legged partridges (51 females and 38 males), which were monitored until October of the
capture year, until death or up to signal loss (until batteries run out). Birds that did not
survive at least 7 days after tagging and those which transmitter failed were excluded
from the analyses. The cause of natural mortality was identified for 35 birds, and was
classified as predation, poaching (hunted out of the game period), and other causes,
including mortality due to agricultural practices (1 case) or unknown causes (3 cases).
Because we were interested in natural mortality, we excluded from our analyses losses
due to agricultural practices or poaching (n = 5) or unknown cases (n = 3).
Genetic analyses
All genetic analyses were performed after fieldwork. Total genomic DNA was
isolated from whole blood using a standard proteinase K/phenol method (Sambrook et
al. 1989). We amplified 8 nuclear microsatellite loci from each sample. We chose the 8
loci for this study from a suite of loci previously developed and screened (Dávila 2005;
Dávila et al. In prep.). A. rufa and A. chukar show different allele sizes at the 8
microsatellite loci, which make them diagnostic genetic markers to assess nuclear
introgression by hybridization between both species. Introgression of the maternally
inherited A. chukar mtDNA into A. rufa was detected by means of diagnostic SNPs
located in the cytochrome b sequence (Blanco-Aguiar 2007). PCR reactions were
performed in a 2720 Thermal Cycler (Applyed Biosystems). Forward primers were
labelled with 6-FAM, NED, VIC or PET and genotyped on an ABI 3100 Automated
Capillary DNA Sequencer. Alleles sizes were determined according to GeneScan 500
LIZ Size Standard (Applied Biosystems) and GeneScan Analysis Software version 3.7
(Applied Biosystems). Digested fragments of cytochrome b were resolved by 2 %
agarose gel electrophoresis and ethidium bromide post-staining.
91
The use of diagnostic markers allowed us to categorically detect chukar

introgression by a simple count of diagnostic alleles at the study loci. We categorised a
bird as “hybrid” when at least one of the genetic markers showed introgression from
chukar, or as “non-hybrid” when none of the markers indicated introgression.
Plasma carotenoid analysis
After collection, blood samples were kept refrigerated until centrifugation (4000
rpm, 10 min). Plasma and cellular fraction separately, were stored at –20 ºC until
analysis. Plasma carotenoid concentration was determined by diluting 60 µl of plasma
in acetone (dilution 1:10). The mixture was vortexed and centrifuged at 10000 rpm for
10 minutes to precipitate the flocculent proteins. The supernatant was examined in a
Shimadzu UV-1603 spectrophotometer at 446 nm (see, for more details, Pérez-
Rodríguez et al. 2007). Finally, plasma carotenoid concentration (µg/ml) was calculated
using a standard curve for lutein (Sigma Chemicals). Lutein was chosen as a reference
pigment because previous works established that this was the main carotenoid circulated
in blood in red-legged partridge (Blas et al. 2006).
Statistical analyses
We used SAS 8.01 (SAS 2001) and STATISTICA 6.0 for statistical analyses.
We used the Princomp procedure (SAS 2001) for the Principal Component Analyses on
biometrics. Dependent variables were checked for normality (Shapiro-Wilk test), and
were fitted to models using the following error distribution: (1) body mass, body size
(PC1; see Table 1), plasma carotenoid concentration, laying date: normal error
distribution and identity link function; (2) clutch size: poisson error distribution and log
function; (3) probability of incubation, hatching success (eggs hatched / clutch size),
probability of hatching young, probability of mortality or predation: binomial error
distribution and logit link function. When analysing variation in body condition, the
dependent variable was body mass, with the first principal component of a PCA
analyses on total body length, wing length, tail length, tarsus length, head width and
beak length (see Table 2), included as a covariate, as an index of body size.
We tested for between years and between sexes differences in proportion of
hybrid and non-hybrid partridges by performing a Chi-square analysis on a contingency
92
Capítulo 3
table. For analyses of breeding performance, we considered each sex separately (see
above).
We estimated survival rate of radio-tagged red-legged partridge during spring
and summer (from early spring to early autumn) using the Kaplan-Meier product-limit
estimator (Kaplan & Meier 1958; Pollok et al. 1989). We used radio-tracking data from
capture until October (throughout the whole study period) or until death or signal loss.
We tested whether variation in survival was explained by year, sex and genotype. Initial
models included sex, year, hybridization and the interactions among these explanatory
variables. We used a backward stepwise selection to eliminate non-significant
interactions or variables from the final model.
We analysed the probability of mortality due to predation including year, sex,
site and hybridization as independent variables, following similar procedure that
described above. All tests were two-tailed.
Table 1. Genetic status (Hybrid/Non-hybrid) of all individuals captured in four game estates during the
study period (2003-2005). Minimum distance (m) from each game estate to the nearest partridge release
point in game estate B (focus of farm-reared red-legged partridge releases).
Game Estate Total
Year A B C D Hybrid/Non-
Hybrid
2003 2/8 11/9 4/5 - 17/22
2004 2/14 8/7 - 0/13 10/34
2005 4/12 - - 2/14 6/26
Total 8/34 19/16 4/5 2/27 33/82
Distance 1688 - 835 9781
RESULTS
Hybridization rate in the studied populations
We found introgression in 33 of 115 birds analysed (28.7 %). The proportion of

hybrids did not differ significantly between sexes (χ² = 1.34, df = 1; P = 0.247; 23.6 %
of males, n = 55, and 33.3 % of females, n = 60) or between years (χ² = 1.46, df = 2; P =
0.482), but differed between game estates (χ² = 16.50, df = 3; P < 0.001). The
percentage of hybrid partridges during the study period was highest in the estate were
93
partridges releases occurred yearly (estate B: 54.3 %), followed by the nearest study
area, where we had evidence of presence of released birds (estate C: 44.4 %), while the
occurrence of hybrid partridges was much lower in the estates where no releases were
performed (19.1 % in estate A, and 7.4 % in estate D; Table 1).
Differences in body size between hybrid and non-hybrid partridges
We used a Principal Component Analysis on all the body measurements to

calculate an index of body size for both males and females (Table 2). The first Principal
Component (PC1) explained 64% of variation, with all the measurements having
positive loadings. The second Principal Component (PC1) explained a further 14% of
variation with tail length having the highest positive loading. PC1 was indicative of
overall size, and was used as an index of body size in subsequent analyses.
Variation in body size (PC1) was explained by sex (F1,103 = 392.04; P < 0.001;
males were larger than females; Fig 1a) and was also significantly explained by the
interaction between sex and hybridization (hybridization: F1,103 = 392.04; P < 0.001;
Hybridization × sex: F1,103 = 4.08; P < 0.05). Body size differed between non-hybrid and
hybrid in males (F1,50 = 4.79; P < 0.05), but not in the case of females (F1,53 = 0.08; P =
0.77). Non-hybrid males were larger than hybrid ones (Fig. 1a).
Table 2. Results of a Principal Component Analysis on biometrics of wild red-legged partridges (n = 107;
Princomp procedure; SAS 2001).
Principal Components
First (PC1) Second (PC2)
Total body length +0.44 +0.31

Wing length +0.43 -0.03
Tail length +0.36 +0.68
Tarsus length +0.42 -0.12
Head width +0.42 -0.25
Beak length +0.36 -0.59
Eigenvalue 3.81 0.86
Variance explained
- cumulative 63.5% 14.3%
- proportion 63.5% 77.8%
94
Capítulo 3
Differences in body condition between hybrid and non-hybrid partridges
Given the sexual dimorphism in size, we analysed variation in body condition

(body mass corrected for size) by sex. In females, variation in body mass was
significantly explained by body size (PC1: F1,51 = 8.73; P < 0.005) and by year (F2,51 =
15.92; P < 0.001), but not by sampling date (linear: F1,50 = 1.62; P = 0.21). Females
were in better condition in 2003 (0.072 ± 0.052) than in 2004 (-0.025 ± 0.069) or 2005
(-0.029 ± 0.042). After controlling for PC1 and year, variation in female body mass was
significantly explained by hybridization (F1,50 = 4.32; P < 0.05), but not by the
interaction hybridization × year (F2,49 = 0.07; P = 0.93). Hybrid females were heavier
relative to their size (better condition) than non-hybrid females (Fig. 1b).
In males, variation in body mass was significantly explained by body size (PC1:
F1,46 = 13.98; P < 0.001), by year (F2,46 = 3.94; P < 0.05) and by sampling date (linear
term: F1,46 = 5.32; P < 0.05; quadratic term: F1,46 = 3.75; P < 0.05). Male condition
increased non linearly with date and was higher in 2003 (0.015 ± 0.051) than in 2004 (-
0.005 ± 0.048) or 2005 (-0.013 ± 0.055). After controlling for PC1, year and sampling
date, variation in male body mass was not significantly explained by hybridization (F1,43
= 0.59; P = 0.45; Fig. 1b), nor by the interaction hybridization × year (F1,43 = 0.34; P =
0.71).
Differences in plasma carotenoid concentration between hybrid and non-hybrid

partridges
Males had higher plasma carotenoid concentration than females (F1,108 = 7.43; P
< 0.01; Fig. 1c). Because of expected differences between sexes in carotenoid use prior
to breeding, we analysed variation in plasma carotenoid concentration by sex.
In females, variation in plasma carotenoids was significantly explained by year (F2,55 =
6.69; P < 0.01) and sampling date (linear: F1,55 = 5.33; P < 0.05; quadratic: F1,54 = 0.08;
P = 0.77). Carotenoid concentration was higher in 2004 (17.03 ± 6.73) and 2005 (19.58
± 6.67) than in 2003 (8.57 ± 4.74). After controlling for year and sampling date,
variation in plasma carotenoids was significantly explained by hybridization (F1,54 =
4.47; P < 0.05), but not by the interaction hybridization × year (F2,52 = 1.32; P = 0.27).
Hybrid females had significantly lower plasma carotenoid concentrations than non-
hybrid females (Fig. 1c).
95
In males, variation in plasma carotenoids was not significantly explained by year

(F2,49 = 0.26; P = 0.77), sampling date (linear: F1,49 = 1.41; P = 0.24; quadratic: F1,49 =
0.04; P = 0.85) or hybridization (F1,49 = 0.12; P = 0.73; Fig. 1c).
Non Hybrid
Hybrid
Females Males
3
a
39
2
13
a)
Size
-1
-2
36 19
-3
b 19
0.04
13
Condition
b) 0.02
0.00
-0.02 39
36
-0.04
c
25
13
41
Plasma carotenoid
39
concentration
20
c) 15
20
10
Figure 1. Differences between sexes and between hybrid (black bars) and non-hybrid (white bars) red-
legged partridges in: a) body size (mean ± SE score of the first Principal Component of a PCA on six
body measurements; see Table 1); b) body condition (mean ± SE body mass corrected for body size, by
sex); and c) plasma carotenoid concentration (in mg.ml-1). Sample size below / above error bars refers to
number of birds.
96
Capítulo 3
Differences in breeding performance between hybrid and non-hybrid partridges
In females, incubation probability did not differ between hybrid and non-hybrid
red-legged partridges (χ² = 0.33, df = 1; P = 0.57). In males, incubation probability
differed between years (χ² = 9.44, df = 2; P = 0.009), and tended to be higher for hybrids
than for non-hybrids (71.42 % ± 18.44 vs 33.33 % ± 9.83; χ² = 3.48, df = 1; P = 0.062).
Laying dates did not differ significantly between hybrid and non-hybrid females (F1,30 =
2.2; P = 0.15). However, hybrid females laid larger clutches (11.78 ± 0.72; n = 9) than
non-hybrid females (9.24 ± 0.55; n = 21; F1,30 = 6.96; P = 0.013), with no significant
differences between years (year effect: F2,30 = 1.48; P = 0.25; year × hybridization
interaction: F1,30 = 0.9; P = 0.35).
Variation in hatching success was not explained by genotype (χ² = 0.81, df=1; P
= 0.35) or by the interaction genotype × sex (χ² = 1.8, df=2; P = 0.17), but was
explained by sex (χ² = 6.51, df=1; P = 0.01). Nesting success in males was higher than
in females (see to similar results chapter 2). Similarly, the probability of hatching
young did not differ significantly between hybrid and non-hybrid birds (χ² = 0.82, df =
1; P = 0.36).
1.0
0.8
Survival
0.6
0.4
0.2
Non Hybrid (n = 63)
Hybrid (n = 26)
0.0
1 2 3 4 5 6 7 8 9 10 11
Month
Figure 2. Mean (± SE) monthly survival probability of hybrid and non-hybrid red-legged partridges (data
from all years and sexes combined). Sample size refers to number of birds.
97
Differences in survival between hybrid and non-hybrid partridges
Survival rate (February to October) differed significantly between hybrid and

non-hybrid birds (Z = 3.37; P= 0.00075; Fig. 2), among game estates (χ² = 19.41, df = 4;
P = 0.00023), tended to differ between years (χ² = 5.92, df = 3; P = 0.052), but did not
differ between sexes (Z= - 0.45; P= 0.65). In the final regression model for censored
data, we only found differences in the survival rate between hybrid and non-hybrids
adult partridges, depending on site (site × hybridization interaction: Wald= 7.64; P =
0.0057). Survival rate was higher for non-hybrid than hybrid birds, but with different
gradients across sites (Fig. 3).
Non-Hybrid
250 Hybrid
21
22 7 4
Mean Partridge Survival Days
200
4 2
11
150 13
100
50
0
A B C D
Game States
Figure 3. Differences in mortality causes between hybrid (black bars) and non-hybrid (white bars) adult
partridges. Data from 2003-2005, February-October.
Predation probability differed between sites (χ² = 9.99, df = 2; P = 0.0068) and

between hybrid and non-hybrid birds, depending on sex (hybridization: χ² = 6.46, df =
1; P = 0.011; sex: χ² = 3.62, df = 1; P = 0.057; sex × hybridization: χ² = 7.63, df = 1; P =
0.0057). Predation occurred in 42.3 % of hybrids birds (n = 26), but only in 23.7 % of
non-hybrids (n = 59). Hybrids males suffered significantly higher predation rate than
non-hybrids ones, but were equally likely to die from other causes. Predators were
mainly carnivores (red foxes, feral cats and feral dogs) and raptors. Hybrids birds (n =
11) were only found predated by carnivores (100 %), while non-hybrid birds (n = 14)
were predated by carnivores (50 %), raptors (28.57 %) or unknown predators (21.43 %).
98
Capítulo 3
DISCUSSION
Our data are the first documenting the occurrence of hybrid red-legged
partridges (A. rufa x chukar) in a wild population during the breeding season. Using
categorical mitochondrial and nuclear markers, we found introgression in 30 % of wild
red-legged partridges. The occurrence of hybrids in our study populations were,
however, within the range of that previously found in shot birds (0-55 % depending on
estates) at a regional scale with a similar method (Blanco-Aguiar 2007).
The occurrence of hybrid partridges was higher in a game estate where more
than 2000 reared-farm partridges are released yearly, and in a nearby population
occupying a similar habitat, than in neighbour populations where releases did not take
place during the last 15 years, a pattern similar to that found at a larger scale (more
hybrid birds in estates where restocking takes place; Blanco-Aguiar 2007).
Releases usually take place in late summer-autumn, and farm-bred birds have a
very low survival rate during the first days after release into the wild (Gortázar et al.
2000; Pérez et al. 2004). Even if few released birds survive, massive releases conducted
over many years in the same area (for instance more than 8 years in game estate B)
would produce a progressive integration of hybrid partridges into wild breeding
populations. Hybrid birds may successfully breed in wild populations, as documented
for the first time by our study, and hybrid females laid larger clutch sizes than non-
hybrid ones. Larger clutch sizes of hybrid birds had been already reported in farmed
birds (Nadal 1992) and the same occurred in the wild. Given that hybrid females had the
same probability of laying a clutch than non-hybrid ones, and similar hatching success,
this would suppose that hybrid females might spread their genotypes more efficiently
than non-hybrid ones. Some of the hybrid birds we detected may have originated from
backcrosses in the wild, but original introgression appeared mediated by human
releases, given that red-legged partridges and chukar partridges do not breed in
sympatry (Del Hoyo et al. 1994). Chukar partridges are not native in Spain, and natural
hybridization areas do not appear to exist (Randi 1996). The confirmation of hybrid
reproduction into the wild highlights threats or concerns for the genetic integrity of red-
legged partridge populations.
Natural hybrid zones of A. rufa x graeca showed a narrower cline than expected,
which could be constrained by natural selection favouring parental species (Randi &
Bernard-Laurent 1999). For hybrids A. rufa x chukar, we do not know how natural
99
selection might act, given their recent presence in the wild. Besides, natural hybrid
populations of Alectoris are restricted to limited parapatric zones, like those along the
border of the southern French Alps (A. rufa x graeca; Bernard-Laurent 1984). In the
case of hybrids between A. rufa x chukar, which are artificial and of human origin, the
contact zones are not limited in space, but widespread across the Iberian Peninsula
(Blanco-Aguiar 2007). The effects of releases and hybridization might differ depending
on prevailing environmental conditions experienced by wild populations. We found that
hybrids survived less well, and suffered higher predation rates in central Spain, which
could limit the spread of hybrid birds into wild populations in the long term.
Nevertheless, there occurrence reported here was high (30%). In contrast, in an
introduced hybrid population on Pianosa Island, in the absence of predators and
hunting, the population increased from 10 pairs to 400 pairs in 20 years (Baratti et al.
2004). The absence of predation may have contributed to this increase in this hybrid
population, more than adaptation to xeric habitat present in Pianosa Island (Baratti et al.
2004).
Differences between hybrid and non-hybrid partridges in body size and

condition
We found differences in several phenotypic traits, depending on sexes, and in

fitness (survival and breeding performance) between hybrid and non-hybrid red-legged
partridges. Non-hybrid males were larger than hybrid ones, while no size difference was
found according to genotype in females. Chukar partridges are larger than red-legged
partridges (Cramps & Simmons 1980), so hybrid birds would be expected to be larger
than non-hybrids, contrary to our results. This could be a result of artificial selection in
captive bred males (see below). Body size often plays a role in intra-sexual competition,
with larger males being favoured in contests. Thus, the larger size of non-hybrid males
may give them an advantage over hybrid males, in terms of competition for territories,
territory size, competition for resources, access to mates, and, in summary, this size
difference could limit the spread of hybrid genotypes from males.
When considering condition (body mass corrected for size), we did not find any
difference between hybrid and non-hybrid males, but hybrid females were in better
condition (relatively heavier) than non-hybrid ones. A better condition is often
associated with greater laying capacity, which could additionally explain the larger
100
Capítulo 3
clutches found in hybrid females. Our results are, at least partly, consistent with those of
a previous study conducted in autumn (during the hunting season, October to
December): hybrid females were found to be in better condition than non-hybrid ones,
but hybrid males were found to be in poorer condition than non-hybrid ones (Blanco-
Aguiar 2007). Here, we did not find differences in body condition between hybrid and
non-hybrid males in spring, possibly because hybrid males in poorer condition in
autumn did not survive overwinter as well as those in good condition (hybrid birds
overall survived less well than non-hybrid birds). An alternative explanation could be
that hybrid males that survived over winter were those able to recover a good condition.
The differences in condition observed in females could be related not only to
hybridization but also to different artificial selection pressures on farm-reared females
aimed at increasing reproductive outputs (Padrós 1991), which have been previously
associated with body condition parameters (Williams 2005). In contrast, small males
could have been selected in order to reduce aggressive behaviour towards females, a
serious management problem in partridge farms (Padrós 1991).
Differences between hybrid and non-hybrid partridges in plasma carotenoid

levels
In birds, carotenoids must be acquired through diet, and are consequently often
limited (Hill & McGraw 2006). Carotenoids play key roles in sexual signalling and
sexual selection by colouring ornaments that function in intra-sexual competition and
mate choice (Hill & McGraw 2006). In addition, carotenoids are beneficial immune
function and for resisting parasites (Blount et al. 2003), and are allocated by females to
eggs for the benefits of offspring (Blount 2004). In red-legged partridges, carotenoid
pigments are responsible for the orange-red colour of legs, eye rings and beak (Blas et
al. 2006; Pérez-Rodríguez 2007). Carotenoid levels also decrease with increasing
intestinal or blood parasite infections as demonstrated in red-legged partridges
(Mougeot et al. MS; Garcia et al. in prep) and other gamebirds (e.g. Martinez-Padilla et
al. 2007; Mougeot et al. 2007). In addition, hybrid birds seem to be more susceptible to
intestinal parasites (Blanco-Aguiar 2007). Thus, lower carotenoid levels might be
indicative of greater parasite infections. Hybrid females had significantly lower plasma
carotenoid concentrations than non-hybrid ones and a possible explanation might be that
they were more parasitized. However, this does not fit with the finding that hybrid
101
females were in better condition than non-hybrid females, given that parasites typically
negatively impact on host condition (e.g. Blanco-Aguiar 2007). Furthermore, no
differences in blood carotenoid levels were found between hybrid and non-hybrid
males. The observed differences might be better explained by a reduced capacity to
absorb carotenoids (captive bred birds have diets poorer in carotenoids than wild birds,
and are less colored), or by different allocation priorities for the available carotenoids,
in hybrid and non-hybrid females. Carotenoids are allocated to eggs (yolk), with much
higher concentrations being found in eggs laid in natural populations than in captive-
breeding farms (Bortolotti et al. 2003). This could have important fitness consequences,
since hybrid females would have less carotenoid available than non-hybrid ones for
sexual ornamentation, for health related function (immune function, parasite resistance;
Mougeot et al. MS) and for allocation to eggs, which has important associated benefits
for offspring fitness, mediated via maternal effects (e.g. Blount 2004). Given that hybrid
females laid more eggs than non-hybrid females, but had less plasma carotenoids prior
to laying, it is possible that they allocated fewer carotenoids to eggs than non-hybrid
females. Differences in carotenoid allocation to eggs between hybrid and non-hybrid
females, and the consequences for offspring fitness, should be investigated in future
studies.
Breeding performance and survival of hybrid and non-hybrid partridges
Our data are the first to document breeding of hybrid partridges (A. rufa x
chukar) in the wild, and to compare the breeding performance of hybrids and non-
hybrids in natural populations. Hybrid females laid larger clutches than non-hybrid
ones. This might be a consequence of artificial selection in farms, with hybrids being
selected for greater reproduction (laying) capacity (Nadal 1992). Larger clutches could
be associated with increased predation risk in birds (Skutch 1982), but we have not
found this to be the case in our population of partridges (chapter 1 and 2). No
differences in laying date, hatching success or nesting success were found between
hybrid and non-hybrid partridges. Red-legged partridge breeding performance has a
marked year-to-year variation (chapter 1), but that variability seemed to affect in a
similar way to hybrid and non-hybrid birds. We also found that hybrid males tended to
incubate more often than non-hybrid ones. Male incubation depends primarily on the
ability of females to lay enough eggs for two different clutches (Green 1984; chapter
102
Capítulo 3
1). This finding is also consistent with hybrid birds being selected for greater
reproduction capacity in captivity. In males, this could be the result of an artificial
selection to reduce aggression in caged mates (Padrós 1991), whenever aggressiveness
and incubation willingness would be opposite traits. The findings that hybrids may
breed as well as, or even better than non-hybrids in wild populations and lay larger
clutches has important implications regarding the persistence and possible spread of
hybrid birds released in the wild.
We found that hybrid partridges survived less well than non-hybrid ones in wild
populations. Hybrid birds suffered additive mortality that was attributable mainly to
predation, in particular by carnivores. Non-hybrid birds were predated mainly by raptors
and carnivores. These results should be interpreted cautiously, given that foxes often
scavenge on dead birds, which could underestimate mortality due to raptors. Predation
is typically the main cause of mortality in farm-reared released gamebirds and
partridges (Leif 1994; Górtazar et al. 2000; Putaala & Hissa 2003), most likely because
of inappropriate antipredator behaviour in captive-bred birds (McPhee 2003). Marked
susceptibility to predators is well known for partridges during the first weeks after
release (Gortázar et al. 2000; Pérez et al. 2004), and our results suggest that this may be
the case in the long-term too.
We found that hybrid birds accounted for c. 30% of breeding birds in a natural
partridge population in Central Spain. Although survival rate was lower in hybrid birds,
enough hybrids seem to survive, recruit and breed for these to be maintained in natural
populations. This might be because despite surviving less well, those hybrids that
recruit might be more productive than non-hybrid birds (greater laying capacity). An
alternative explanation is that there is a continuous reinforcement of hybrid birds into
wild populations because of repeated (annual) and massive (3-4 millions / year in Spain)
releases of captive bred-birds into the wild, with poor or no genetic control. There could
also be an important risk of hybrids spreading into populations where no releases take
place, or hybrids becoming established in the long-term after releases, as shown by
hybrid presence, although in lower frequency, in game estates where releases have not
been performed since at least 15 years ago. Blanco-Aguiar (2007) also found hybrid
birds in game estates that do not release birds as a management tool. This raises
103
concerns about the risks and scale of introgression into the “pure” wild partridge
populations. According to Spanish Law 4/1989 for the Conservation of Natural
Landscapes and Wild Fauna and Flora, the release of alien species and hybrid animals is
strictly forbidden, but our results are clear evidence of the poor implementation of that
law. Therefore, controlling the introgression of allochthonous genomes is a piece of
vital importance to assure long-term persistence of wild “true” red-legged partridge
populations. Our results definitely confirm the concerns about genetic problems that
raised the status of “vulnerable” for this species (Aebischer & Potts 1994). It could be
thought that the easiest and fastest way to solve this situation could be to forbid
releases. However, our results suggest that the current genetic status of Spanish
partridge populations could worsen in the long-term even if releases were stopped,
given that hybrid birds already breed in the populations. Thus, the management strategy
should not be stopping releases, but recovering the original genetic structure of
populations by the same method that drove them to their current status, that is, releases
with genetically pure partridges. For that reason, and mostly in accordance with
suggestions by Blanco-Aguiar (2007), we may recommend: (a) Implementation of a
serious inspection protocol of partridge farms and game estates where partridge releases
are performed, stopping releases of hybrid birds, and identifying areas where
management actions should be implemented to correct the genetic status of populations;
(b) Where necessary, implementation of restocking programs with “pure” red-legged
partridges, associated with intensive hunting to remove hybrid birds, trying to recover
the original genetic pool of the species; (c) Cataloguing important areas for the
conservation of genetic purity of red-legged partridges, with particular reference to the
largest continuous areas where restocking programs have not been performed by now,
and promoting management plans to avoid releases in those areas (see Blanco-Aguiar
2007 for a complete recommendation list).
The low effectiveness of farm-bred gamebird releases as a management tool has
been demonstrated in several species (Leif 1994; Gortazar et al. 2000; Putaala & Hissa
2003). Additionally, evidence of negative effects of small game releases over other
species that share the same habitat has been accumulated over last decades. Intensive
hunting based on large-scale releases of red-legged partridges could have contributed to
the local extinction of grey partridge Perdix perdix in the UK (Watson et al. 2007),
Although grey partridges are considered a quarry species, their populations have
suffered such large declines that traditional shooting became not worthwhile (Aebischer
104
Capítulo 3
1997). Interespecific parasitic transmission also is a problem for biodiversity

conservation (Tompkins et al. 2001; Villanúa et al. 2007). Gamebird releases affect not
only the species released, but also others inderectly, because of overhunting (Keane et
al. 2005), transmission of new parasites (Villanúa et al. In press), which are causes for
more concerns.
ACKNOWLEDGEMENTS
We thank all game managers and hunting societies´ presidents, especially to

Inocencio Bastante, Lorenzo Sobrino, Delfín Martín de Lucía and Jose Juan Bermejo
for allowing studying partridges on their hunting estates. Particular thanks are due to
Ambrosio Donate, Salvador Luna, Gustau Calabuig, Antonio Linares, Jesús Martínez-
Padilla, Laura Iglesias helped with the data collection. F. Casas was supported by a pre-
doctoral grant of the Junta de Comunidades de Castilla la Mancha (JCCM). This work
also received financial support from the research project “Bases científicas preliminares
para un plan de conservación de la perdiz roja en Castilla-La Mancha” of the Consejería
de Agricultura y Medio Ambiente de la JCCM (Junta de Comunidades de Castilla-La
Mancha), and CYCIT projects MCYT-REN200307851/GLO and CGL2004-
02568/BOS. FM was supported by a NERC advanced fellowship, a Grant from the
Ministerio de Educación y Ciencia, Spain (CGL 2006-11823) and from the JCCM,
Spain (PAI06-0112).
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CAPÍTULO 4
Distribución a escala local de los linajes de malaria aviar entre

poblaciones de una especie hospedadora: ¿Un efecto no deseado e
infravalorado de una extendida práctica de gestión?
García, J.T., Casas, F., Calero-Riestra, M. & Viñuela, J. Small-scale spatial distribution of avian
malaria lineages between populations of a resident host: overlooked and unwished effect of a
widespread human management practice? Molecular Ecology, en evaluación.
Capítulo 4
ABSTRACT
1. With the application of molecular-based protocols, recent advances have been

done in our knowledge of how avian malaria parasite prevalence and community
structure vary over time and space. However, the genetic structure of such
parasites at small spatial scale remains poorly explored. At this study-scale,
anthropogenic changes on the environment, such as local introduction of
parasites in the wild via releasing farm-reared birds could influence parasite
evolution, host population dynamics, and host-parasite interactions.
2. We examined the distribution of avian malaria parasites infecting resident avian
hosts (red-legged partridge Alectoris rufa) at local scale, with particular
emphasis on the effect of human activity (releasing farm-reared birds for hunting
purposes) on the spatial structure of lineages. We found an unusually high
prevalence (50 %) of Plasmodium spp., and substantial differences in spatial
distribution of lineages among the four populations studied.
3. While some closely-related parasite lineages achieved high occurrence in game
estates without introduced farm-reared partridges, other lineages followed the
opposite pattern, being more abundant in game estates with releasing activity
than in sites without released birds. Indeed, one lineage previously recorded in
other avian hosts appeared exclusively in game estates with releasing activity,
whereas the dominant lineage showed higher occurrence in non-restocking
populations.
4. Synthesis and applications. Our results support the hypothesis that local
introduction of gamebird species is an important factor affecting parasite
distribution at local scale. Assessing the consequences of human management on
hosts is essential to understanding the implications of such phenomenon for
wildlife conservation and disease control.
INTRODUCTION
The interest on parasite-host relationships and their effects on wild animal

populations are currently spread across many disciplines such as evolutionary biology,
ecology, parasitology, behavioural sciences, wildlife management and conservation
biology (Hamilton & Zuk 1982; O’Brien & Evermann 1988; Møller 1997; Hudson et al.
2002; Bensch et al. 2007), because parasites and infectious diseases can largely affect
life history traits of their hosts (Price 1980; Loye & Zuk 1991; Lively & Dybdahl 2000).
Recently, the application of molecular-based protocols has widened our knowledge
about parasite diversity in wild populations of hosts. In particular, the application of
such methods to the study of avian malaria (Haemoproteus and Plasmodium) has
revealed an extraordinary degree of genetic diversity in natural populations (Ricklefs &
Fallon 2002; Waldenström et al. 2004; Bensch et al. 2007). Due to this remarkable
genetic variation, along with the high degree of host specificity (Bennett & Peirce 1988;
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Bennett et al. 1994; Bensch et al. 2000), avian malaria parasites have become a
powerful model for the study of ecology and evolution of parasites and their hosts
(Lively & Dybdahl 2000; Pérez-Tris et al. 2007). Avian malaria is the most widespread
and genetically diverse vector-transmitted avian disease, having potentially negative
effects on the survival and fitness of several avian species (Atkinson & van Riper 1991;
Valkiūnas 1993; Merino et al. 2000). Recent studies indicate that genetically
differentiated lineages of avian malaria may display different pathological effects on the
same hosts (e.g. Bensch et al. 2004), due to differences in pathogenicity among parasite
lineages and/or differences in host susceptibility (Foster et al. 2007). Therefore,
important recent advances have been done in our knowledge of how prevalences and
community structure of parasites vary over time and space (e.g. Fallon et al. 2005;
Wood & Cosgrove 2006; Kimura et al. 2006; Bensch et al. 2007), on the ability of
parasites to disperse among hosts (Pérez-Tris & Bensch 2005), or on host resistance to
parasite lineages (Westerdahl et al. 2005). However, the genetic structure of parasites at
small –local– spatial scale remains poorly explored (Fallon et al. 2005), despite their
potential in determining local prevalences, dispersion patterns, and thus, parasite
virulence and pathogenicity of different lineages.
Moreover, the influence of humans in host-parasite complex have been
traditionally overlooked, although human-induced environmental changes may
profoundly alter the spatial genetic structure of parasite and host populations, as
recently reviewed in a compelling monographic issue of Molecular Ecology (January
2008). For example, the introduction by humans of parasite species into new
environments can largely influence parasite evolution, host population dynamics, and
host-parasite interactions (Benkman et al. 2008; Smith & Bernatchez 2008; Villanúa et
al. in press), and growing empirical evidence indicates that this kind of human-induced
changes are more common than previously thought (Smith & Bernatchez 2008). In this
context, management of some wild species for hunting purposes are crucial cases in
which human actions may be modifying at large scales genetic structure, community
composition, and life histories of both parasites and hosts (Gortázar et al. 2006; Randi
2008). Gamebirds, particularly red-legged partridges (Alectoris rufa), provide a
particularly interesting model for this purpose. This gamebird is a medium-sized
Phasianidae native from the Iberian Peninsula that has suffered a sharp decline in their
wild populations during the last decades (Hagemeijer & Blair 1997). Small-game
hunting in Spain (mainly based on rabbits Oryctolagus cunniculus, and red-legged
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partridges) generates an economical movement of more than 210 millions of euros each
year in Spain. As a consequence of the great demand for partridges to hunt, along with
the scarcity of birds in the wild, more than 4 million farm-reared partridges are
estimated to be released yearly for hunting activities in Spain (Garrido 2002). The
number of released bird that survive after their first “hunting season” (from august to
January) is potentially low (Gortázar et al. 2000; Alonso et al. 2005), but successful
settlement and breeding in the wild of released partridges has been proved (Duarte &
Vargas 2004). The possibility of released partridges dispersing intestinal parasites into
wild populations, as well as transmission of new parasites to other sympatric bird
species have also been reported, and the potential effect of these parasite introductions
should not be negligible (Millán et al. 2004a, b; Villanúa et al. in press). To our
knowledge, no specific pharmacological treatments for blood parasites in farm-reared
partridges are used at all in Spain, although the rutinary management of partridge-farms
(very high densities of animals and increased stress factors) may be particularly
favourable for the propagation of malaria parasites (authors, unpublished data). After
releasing partridges into the wild, the increased density of individuals at local scale
could increase intra- and inter-specific contacts between infected and uninfected
individuals, optimal conditions for propagation of parasites into new environments.
Such a phenomenon may indeed be of great conservation concern, since although local
introductions of parasites may be innocuous; they could also modify the evolutionary
course of parasite communities, affect viability of wild or released partridges, or even
cause local extinctions (Warner 1968; van Riper et al. 1986). Besides, the potential
impact on hosts derived from local introduction of new parasites remain poorly studied,
but it is expected to cause high mortality rates, because natural populations should have
lower resistance towards parasites to which they have no previous contact (Newton
1998).
Here we examine the spatial distribution of avian malaria populations infecting
wild resident red-legged partridges at a local scale, in four populations of red-legged
partridges. The four study areas follow contrasting game management models, from no
releases to intensive hunting of released partridges. Our aim was to characterize avian
malaria parasites in the four populations in central Spain, determining the spatial
distribution and abundance between lineages, and thus the capacity of each malaria
lineage to disperse among host populations. We also examined the effect of human
activity (releasing farm-reared birds) on the spatial distribution of avian malaria
115
lineages, discussing the implications of such phenomenon for wildlife conservation and
disease control.
Figure 1. Sampling sites around Ciudad Real city, central Spain. The four host populations studied were
indicated by different colours.
MATERIALS AND METHODS
Study populations and field procedure
The study area comprises 125 km² located in Campo of Calatrava region
(Central Spain, 38º 80´ N, 3º 80´ W, 610 m a.s.l.). The climate is Mediterranean with
marked continental character, reflected in dry and hot summers, and moderately wet and
cold winters. Habitat is characterized by undulated farmland mainly aimed to cereal
cultivation (mostly barley), with interspersed patches of olive groves, vineyards, dry
annual legume crops (mainly vetch Vicia sativa) and sugar beet (Beta rubra). Natural
vegetation areas are very scarce, limited to a few parcels of pastureland and fallow, and
small patches of Mediterranean scrub, mainly on the top of hills. We obtained adult red-
legged partridges blood samples in early spring (February and March) during 2003-
2005 from 4 sampling sites 1,8-11,1 km-distant (game states A, B, C, and D, Fig.1). The
four sampling sites had similar landscape, but differed markedly in game management
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Capítulo 4
systems. One of the game estates sampled (B) followed an intensive management model
with more than 2.000 farm-reared partridges released each year. In game state C farm
partridges were also detected in the field in lower numbers and more sporadically,
probably came from game estate B (see results chapter 3). Finally, game states A and D
followed a traditional management model without restocking with captive-bred game
birds since more than 8 years ago (chapter 3). A total of 115 adults were caught under
license using cage traps with an alive decoy (adult red-legged partridge inside the cage),
and baited with wheat.
Avian malaria diagnosis
Blood samples were obtained by ulnar venepuncture and stored in 99% ethanol
until molecular analysis. DNA was extracted from samples using standard NH4Ac
methods, and diluted to a working concentration of 25 ng/ml. We first evaluated the
quality of extracted DNA by electrophoresing 2 µl of the extract in 2% agarose stained
with ethidium bromide, and visualizing it under UV light. The samples were screened
for the presence of Plasmodium and Haemoproteus using nested polymerase chain
reactions (PCR) protocol (Waldeström et al. 2004), designed to amplify a 479-bp
fragment of the mitochondrial cytochrome b gene of both parasite genus. The PCR tests
were performed in two separate runs with positive (i.e. DNA from individuals with
known malarial infections) and negative (ddH2O) controls. Pre- and post-PCR work
were performed with different material and in different sections of the laboratory to
avoid contamination.
The method started with a pre-amplification using primers located outside the
target fragment (HaemNF and HaemNR2), followed by a final amplification with the
primers HaemF and HaemR2 (Bensch et al. 2000). In both steps, PCR reactions were
set up in 10 µl total volumes including 50 ng of templateDNA (1 µl of pre-amplified
PCR product in the second reaction), 1xPCR buffer (Biotools), 0.125 mM of each
nucleotide, 0.4 mM of each primer, 1.5 mM MgCl2, and 0.25 units of Taq DNA
polymerase (Biotools). Reactions started with 3 min at 94 ºC, followed by 20 cycles
(first step) or 30 (second step) of 30 s at 94 ºC, 30 s at 50 ºC and 45 s at 72 ºC, and they
were terminated by a 10-min extension at 72 ºC. We evaluated 2.5µl of each final
reaction on 2% agarose gels stained with ethidium bromide and using 1xTAE buffer.
We repeated the protocol three times to confirm negative infections. All samples with
117
positive PCR reactions were successfully sequenced from both ends. We used the
MicroSpin s-400 HR columns (Amersham Biosciences) to purify PCR products, which
were sequenced from both ends using a Big Dye Terminator Kit. The sequencing
reactions were cleaned on standard Sephadex columns, and DNA sequences were
determined using an ABI 3130 automated sequencer (Applied Biosystems). Reading
data were processed with the ABI PRISM1 Sequencing Analysis Software v3.7
(Applied Biosystems).
Defining parasite lineages
We aligned and edited DNA sequences using Clustal W (Thompson et al. 1994)
and Bioedit (Hall 1999), with published sequences of other avian malaria parasites
registered in GenBank. Because many of the sequences differed by only few sites of the
479 examined, and some avian malaria cyt b lineages with less than 0.5% sequence
divergence may represent different species (Bensch et al. 2004), the same person (JTG)
examined carefully each sequence at least twice, discarding sequences with ambiguous
sites (then amplified and sequenced again) to assess the quality of the sequences. Here,
we used a sequence divergence of at least one nucleotide to define lineages
(Waldenström et al. 2002).
Although we did not have information on the morphological identity of our
lineages, different Plasmodium and Haemoproteus morphospecies have been
genetically characterized, and recent works have linked morphospecies and molecular
sequences (e.g. Valkiūnas et al. 2007). Despite different lineages representing the same
morphospecies often diverge in molecular sequence and probably may represent truly
different species (Bensch et al. 2004), the cyt b sequences of most morphological
species of avian Haemosporidia are clustered together into monophyletic clades
(Beadell et al. 2006; Martinsen et al. 2007; Valkiūnas et al. 2007). Therefore, we tested
whether malaria lineages isolated from our hosts could correspond to one or more
morphological parasite species by constructing a phylogeny including published
sequences of parasites identified by morphology (8 sequences from 7 morphospecies of
Plasmodium, and 6 sequences from at least 3 different Haemoproteus morphospecies).
Then, we explored the clustering of our lineages, which were assigned to a given
morphospecies when included into the same monophyletic clade. Phylogenetic
relationships among parasite lineages were estimated using different primate malaria
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Capítulo 4
sequences (Plasmodium vivax GenBank accession no. AF069619, Plasmodium

malariae GenBank Accession nº AF69624, and P. reichenowi AF069610) as outgroups
to root the tree. We used PAUP* 4.0 (Swofford 2002) to construct a maximum
likelihood (ML) phylogenetic tree of all cytochrome b lineages. We performed the
model of nucleotide substitution that best fitted the data (selected among 56 models
tested by PAUP*), as determined using the Akaike Information Criterion (AIC)
implemented in Modeltest 3.7 (Posada & Crandall 1998). To build the ML tree, we
conducted a heuristic search and using a tree bisection reconnection (TBR) algorithm
for branch swapping, with random addition of sequences. The statistical support for
internal branches of the tree was estimated by 1,000 bootstrap replicates. We also used
neighbor-joining (NJ) and maximum parsimony (MP) tree reconstruction methods to
ensure consistency of the results.
Following the reasoning described above, we analysed the genetic structure of
our parasites pooling together lineages that resulted monophyletic with respect to
morphological species in all phylogenetic analyses. We used analysis of molecular
variance (AMOVA; Excoffier et al. 1992), considering Tamura and Nei distance
method (Tamura & Nei 1993), under a gamma distribution with α = 0.14, which was
estimated from the data by Tree-Puzzle 5.0 (Schmidt et al. 2002). We tested for two
alternative scenarios: (1) genetic structure resulting from differentiation among the four
sampling game estates, and (2) differentiation among game estates with released birds
(sites B, and C) and those that maintain only natural wild populations (A, and D). The
statistical significance of genetic variation was estimated using Monte Carlo simulations
with 5,000 permutations of parasite haplotypes among populations (Excoffier et al.
1992).
Statistical analysis
We used Fisher’s exact tests to analyse whether haplotype proportions at each

population deviated significantly form a null expectation of random distribution among
sites. We also analysed variation in the spatial distribution of lineages in relation to
hunting management models in host populations. For this purpose, we grouped together
those malaria lineages that tentatively belonged to the same species (resulted from the
ML phylogenetic tree, see above), and built a log-linear analysis with two-factors,
“species” (clades a, and clade b, see below) and the type of hunting management
119
(releasing partridges, non releasing partridges). All analyses were done using Statistica
6.1 software (StatSoft 2002).
RESULTS
Malaria infections were detected in 52 individuals out of 112 Red-Legged

partridges screened from 4 study areas, which represent an overall 46.4 % of prevalence
in the host population (Table 1). All parasite cytochrome b lineages examined
correspond to Plasmodium spp. (Fig. 2), whereas sequences belonging to Haemoproteus
spp. were absent in our sample set. Eight unique Plasmodium cytochrome b lineages
were defined by 43 variable nucleotide sites. There were no insertions or deletions, and
thus the nucleotide alignment was unambiguous.
Table 1. Malaria (Plasmodium sp.) parasite lineages recorded within 112 samples of red-legged
partridges in four study sites in central Spain. Data shown as percentage of infected birds by lineages, and
total prevalence within each population studied.
Populations
Parasite taxon Lineage GenBank A B C D Prevalence (%)
Plasmodium sp. ARF1 EU395835 11 2 3 11 51.9
Plasmodium relictum SGS1 AF495571 7 3 2 1 25.0
Plasmodium relictum GRW11 AY831748 0 2 1 0 5.7
Number of birds captured 39 35 9 29

Number of infected birds 21 9 7 15
Percentage of infections 53.8 25.7 77.7 51.7
Two of the haplotypes found in red-legged partridges (SGS1 and GRW11) have
been previously recovered in other avian hosts. The remaining six haplotypes have
never been previously registered in any other avian host, showing variable differences
(between 0.2% and 2.3%) with any known Plasmodium cytochrome b lineage recovered
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Capítulo 4
in avian hosts. The most common lineage in our samples was ARF1 (52% of detected
haplotypes), followed by SGS1 (25%), ARF6 (9.6%), and GRW11 (5.7%). The
remaining four haplotypes (ARF3, ARF5, ARF7 and ARF9) were only detected in
single individuals (1.9 % of detected haplotypes), and thus may be considered
anecdotical infections by lineages depending on other host species (Bensch et al. 2007).
Sequence divergence between lineages varied from 0.2% (1-bp substitution between
SGS1/GRW11 and ARF2/ARF9) to 7.8% (ARF7/ARF3). The two commonest lineages
(ARF1 and SGS1) in our study are more divergent in the cytochrome b gene than are
the human and chimpanzee parasites P. falciparum and P. reichenowi (Escalante et al.
1998). Furthermore, lineage ARF7 exhibited much larger differences with respect to all
other lineages (range 6.7 - 7.86 %).
Malaria lineages of red-legged partridges
Although we did not have morphological data of parasites found by molecular

methodology, according to the sequence divergence matrix our lineages seem to
correspond to, at least, three well differentiated species (Bensch et al. 2004). This
divergence among potential species was also supported by the phylogenetic
relationships between cytochrome b lineages. We built a ML tree (Fig. 2) assuming a
GTR+I+G model of nucleotide substitution, which supported the existence of three
separate groups of lineages. Other tree reconstruction methods (NJ and MP) produced
the same topology. Three of the haplotypes found (ARF1, ARF3, and ARF6) clustered
together into a well-supported clade (clade a; Fig. 2), which did not contain sequences
of any of the morphospecies included in the analysis. All phylogenetic analyses
supported this cluster as a sister-clade of Plasmodium relictum sequences (clade b; Fig.
2). Our isolates SGS1, ARF5, GRW11 and ARF9 did fall together into the P. relictum
clade and then, we tentatively consider these lineages as belonging to the same species
(P. relictum) for further analyses. Likewise, our isolates ARF1, ARF3, and ARF6 were
pooled together for statistical analyses (see, however, problems with this reasoning in
the discussion). Finally, ARF7 did not match any described morphological species and
was placed in the resulted phylogeny close to Plasmodium rouxi species, thus
corresponding to a very different species.
121
Figure 2. Maximum likelihood phylogenetic tree showing the phylogenetic position of malaria parasites
found in red-legged partridges sampled in central Spain (four populations). Published sequences of other
Plasmodium and Haemoproteus species (GenBank accession numbers are indicated in the tree) have been
used to construct the phylogeny. Results derived from ML analysis of cyt b sequences (479 bp) under the
GTR+I+G model of nucleotide substitution. Support to internal branches based on bootstrap replicates is
indicated by numbers when larger than 50% (1000 replicates). The tree was rooted with sequences from
three primate malaria species (P. vivax GenBank accession no. AF069619, P. reichenowi GenBank
accession no. AF06961, and P. malariae GenBank accession no. AF069624). Sequences grouped in
clades that should correspond to different parasite species (clade a, clade b, and lineage ARF7) are
indicated by colours as those in Fig.3.
Variations in lineage distribution among populations
We found red-legged partridges infected by Plasmodium in all the four sampled

populations. The highest parasite prevalence was found at site C, with 77 % of birds
infected, whereas “site B” had the lowest (26% of birds infected, see Table 1). The
frequencies of the eight lineages isolated in red-legged partridges were not randomly
distributed among sampling sites (Table 1; Fig. 3), suggesting a differential probability
of transmission of lineages among populations. Among infected birds, lineage ARF1
clearly dominated the parasite community in three of the four populations studied,
although a large between-population variation in the occurrence of each lineage was
observed (see Fig. 3). Even when considering only lineages present in all the four
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sampling sites (ARF1 and SGS1), large differences in the relative frequency of
occurrence among host populations were apparent (Fig.3). Tentatively, and considering
isolates from the same clade as belonging to the same species, the frequency of
occurrence also varied among game estates, ‘clade b’ representing the 55% and 57% of
infections in game estates B and C, while only 38% and 7% in game estates A and D,
respectively. Infections corresponding to parasites from clade a represented 93% of total
infections in population D, 57% in population A, 44% in population B, and 43% in C.
These differences resulted significant for parasites belonging to ‘clade a’, that reached
higher occurrence in game estates without introduced farm-reared partridges than in
game estates with releases (Fisher exact P = 0.036), while ‘clade b’ followed the
opposite pattern, as it was less frequently found in game estates without releasing
activity than in sites with releasing activity (Fisher exact P = 0.04). Despite of reduced
power for geographic effects due to small sample size (1 to 8 samples in each of the
four game estates for clade b, and 3 to 14 for clade a), the log-linear analysis of
prevalence according to the type of hunting management (releasing partridges vs. non
releasing partridges) and parasite clade produced a significant model (partial
association: χ² = 6.96; P = 0.008). These findings suggest that human introduction of
red-legged partridges in the field is an important factor affecting parasite distribution at
local scale. Indeed, it is also noticeable that one of the two lineages previously recorded
in other avian hosts (GRW11) appeared exclusively and in similar proportions in the
two game estates with farm-reared partridges (Table 1; Fig. 3), but was absent in game
estates without restocking with captive-bred game birds. Furthermore, the commonest
haplotype (ARF1) showed higher occurrence in non-restocking populations than in
bird-releasing populations (Fisher exact P < 0.001; Fig. 3).
There was no geographic structure (n = 4 populations) in the genetic variation of
lineage parasites belonging to clade b (P. relictum) (AMOVA: ФST = -0.01; df = 3.17; P
= 0.44, estimated genetic variance among populations = 0). In contrast, the AMOVA
analysis testing for differences in genetic structure (clade b) in relation to type of
management explained a considerable proportion of total molecular variance (25.38%),
although results were non-significant, possibly as a consequence of small sample size
(population D, for example, had only one sequence belonging to clade b, see Table 1).
Such a tendency of geographic structure depending of the releasing activity was also
evident from the pattern of pairwise tests of population differentiation, comparisons
involving populations A and B resulting in nearly significant ΦST value (P = 0.09).
123
When population D (n = 1) was excluded from the analysis, population pairwise ΦST
value became significant between populations A (without introduced partridges) and B
(with farm-releases birds) (pairwise ΦST = 0.17; P = 0.01), the two populations with
larger sample sizes (n = 8 and n = 5).
Figure 3. Spatial distribution of malaria lineages found in resident red-legged partridges in central Spain.
Pie charts indicate the proportion of all sequenced Plasmodium infections in a given population (the four
host populations are labelled by different colours as in Fig. 1). The relative frequencies of the two clades
with good support in phylogenetic analyses are represented by histograms (colour-coded as in Fig.2 to
help identification). Lineage ARF7 (yellow bar) is present in only one population.
DISCUSSION
We obtained two main interesting results on relevant issues in the study of host-
parasite systems: (1) an unusual high prevalence of Plasmodium in resident hosts
inhabiting open Mediterranean landscapes, and (2) differences in local distribution of
lineages among populations of a single host species, which may be indicative of a
differential effectiveness in malaria transmission between areas, or a possible negative
consequence of human gamebird releases.
124
Capítulo 4
In the only previous studies about hemoparasites in red-legged partridges,

developed by the classical technique of identifications in blood smears, Encinas (1982)
found a lower prevalence of P. relictum in wild birds of western Spain in the late 70s
(3.2-16.6 %, depending on the sampling method), and Millán et al. (2003) found 10 %
of prevalence of Haemoproteus spp. in farmed birds. The large differences in malaria
prevalence between these studies on the same host could be due to different infestation
rates between areas, to differences in the detection efficacy of research protocols (blood
smears vs. genetic identification); or may be indicating that wild partridges are locally
well adapted to Plasmodium parasite community, holding the host populations low
levels of parasitism more readily found by molecular techniques than by microscopic
examination of blood smears (Waldenström et al. 2004). Furthermore, we can not
discard a possible real increase in parasite prevalences along last decades, due to an
effect of widespreading game releases (see below).
Studies on bird species living in open arid or semi-arid environments have
detected hemoparasite prevalences usually lower than 20 %, and often near 0 (Little &
Earlé 1995; Valera et al. 2003). Contrary to this pattern, the high rate of infested birds
observed in this study is similar to those recorded for other gallinaceous birds in tropical
or subtropical environments (e.g. Earlé & Little 1993), but markedly higher than those
recorded in birds living in open and arid environments. This pattern is now open to
debate as a result of the use of molecular techniques to examine parasite infections,
which usually provide higher prevalences than the traditional microscopic examination
of blood smears (e.g. Wandelström et al. 2004). However, some recent studies using
molecular techniques still reported low prevalences in birds of arid environments. For
example, Ortego et al. (2007) found, using the same diagnostic protocol than this study,
less than 15 % of lesser kestrels Falco naumanni infected by malaria parasites
(Plasmodium and Haemoproteus) in central Spain (La Mancha), an area nearby to our
study area and with similar landscape features. The lesser kestrel is a migrant and
colonial breeder that should theoretically reach higher prevalences than our hosts
(resident and territorial), since transmission rates should be higher in breeding colonies
than in territorial breeders (Tella 2002) and the ‘migrant’ character of the host should
favour a wider array of parasites than in resident species (Pérez-Tris & Bensch 2005).
The absence or low prevalences of hematozoan found in hosts inhabiting open and arid
environments has been commonly attributed to a reduced transmission rate due to the
scarcity of suitable vectors (review in Martínez-Abrain et al. 2004). Our findings at this
125
respect (almost 50 % of infected birds) suggests that abundance of appropriate vectors

in open and summer-drought regions seems not to be a determining factor for the
existence and dispersion of malaria parasites. Other factors could also underlie
differences in parasite prevalences among different host-parasite assemblages living in
similar landscapes, such as different immunological capabilities of the hosts or different
virulence of lineages sampled (de Roode & Read 2003), population density of hosts (but
see Keymer & Anderson 1979), within-host competition among closely related parasites
(Martinez-Abrain et al. 2004; de Roode et al. 2005), or different mortality rates among
infected individuals (Bensch et al. 2007). Finally, we can not discard that the high
prevalence we have found may be due, at least partially, to an ongoing increase in
prevalences of haemoparasites in wild partridges due to widespread farm-bred partridge
releases over the last decades, as also suggested by spatial distribution of lineages (see
below). Larger scale studies are urgently required to explore this possible negative
influence of that management technique.
We have detected a non-random distribution of Plasmodium lineages infecting
hosts from different populations. Three lineages (ARF1, SGS1, and ARF6) were
broadly distributed among the populations studied, whereas four lineages were
restricted to single populations. Indeed, two of the haplotypes found in red-legged
partridges (SGS1 and GRW11) have been previously recovered in other avian hosts,
suggesting low host-specificity for these lineages, broad geographic range and a
probable high potential for local adaptation (described for SGS1, see e.g. Pérez-Tris &
Bensch 2005, and Bonneaud et al. 2006). The fact that malaria lineages had different
spatial distributions within the same hosts in a small geographic area supports the idea
that ecological differences between parasites yield unequal ability to achieve high
occurrence or different dispersal rates even at a very small geographical scale (Pérez-
Tris & Bensch 2005). Such a result might also be attributed to the relationship between
parasite pathogenicity and host resistance if, for example, different parasite lineages
cause different mortality rates among infected individuals reducing the abundance of
alive birds with a given lineage (Bensch et al. 2007), or if the immune system of hosts
responds in a different way to each lineage. Genetic diversity may affect the ability of
species to evolve resistance to malaria (Foster et al. 2007), and recent studies have
found important associations between malaria and MHC genes (Major
Histocompatibility Complex) of their hosts (Westerdahl et al. 2005; Bonneaud et al.
2006; Loiseau et al. 2008) that could help explain differences in susceptibility to
126
Capítulo 4
infections between populations of the same host. Such pattern of malaria distribution at
local scale demonstrate, in any case, that low-scale distances and relationships among
host populations should be more carefully considered in future studies of host-parasite
complex, at least in resident hosts with low dispersal rates, such as red-legged
partridges. Differences in malaria prevalence between nearby sites suggest that infection
probability may depend to a greater extent on factors such as natal site, dispersal rates
and the choice of breeding places, highlighting the importance of horizontal
transmission at local scale, and enhancing the possible negative influence of human
intervention. Under these circumstances, and taking into account the observed
differences in malaria distribution between natural host populations and those managed
by humans, alien (human-introduced) parasites may intensify disease impacts on
populations, particularly in species such as red-legged partridges that are sedentary
territorial animals showing only short range movements and dispersal (Del Hoyo et al.
1994; authors, unpublished data), specially in released farm-bred birds (Alonso et al.
2005). A human-induced increase in prevalence or diversification of parasite
community, would induce new immune challenges in wild bird populations (de Roode
et al. 2005), maybe jeopardizing other host’s life history traits. In our case, the situation
could be even worse than the one we are reporting, since it is probable that lineages
isolated in this study, and considered the same species in our analyses, could in fact
correspond to different malaria species (cryptic species may differ by just 0.4% in the
cytochrome b sequence; Bensch et al. 2004).
The effects of the introduction of parasite species into new environments may be
especially difficult to detect without field studies prior to introductions (see Beckman et
al. 2008 for a recent review). Thus, the adverse effects of releases for local genetic
diversity of parasites are likely to go unnoticed. Gamebird releasing is a very usual
activity in many places of the world, and the potential effect of introduction of parasites
into new environments should not be discarded, on the contrary, should be increasingly
considered in evolutionary studies. Like free-living organisms, parasites and pathogens
can colonize and evolve in new environments, and humans routinely serve as dispersal
agents (Mack et al. 2000) creating novel habitats for parasites that, in turn, function as
ongoing sources of infection for other individuals or species. For example, humans are
127
responsible for the introduction of mosquitoes and associated pathogens in different

countries, leaving dramatic examples of bird extinctions on islands (Warner 1968; van
Riper et al. 1986; Atkinson et al. 1995), due to the consequences of the first exposure of
native birds to infections (Van Ripper et al. 1986; Atkinson & Van Riper 1991).
Evidences concerning the effects of blood parasites in wild non-passerine birds are
however limited, and in red-legged partridges absent. We have found, for the first time,
evidence suggesting the influence of game-releasing activity in malaria spatial
distribution at local scale. Our results indicates that common malaria lineages detected
in other bird species (SGS1, GRW11), as well as other closely -related lineages found
for first time in this study, infected more hosts in areas where game-releasing activity is
performed than in wild populations, whereas the opposite pattern was found for malaria
lineages not detected previously in other avian hosts. Tens of million gamebirds are
released yearly in Europe (Viñuela & Arroyo 2002), and our results with blood
parasites, as well as previous works with intestinal parasites, strongly suggest that the
potential effect of releases promoting introduction of parasites into new environments
should be more carefully considered, and further studies are urgently required. Indeed,
the effects could also be extended to sympatric species, some of which may be under
conservation concern (Villanúa et al. 2007). Extended survey of blood parasites in
commercial partridge farms using molecular techniques must be considered as an urgent
research and management priority for disease control and wildlife conservation. More
studies involving large sample sets and possible pathological effects of malaria are
needed to asses adequately the consequences of human management of host populations
in explaining the geographic structure in genetic parasite variation.
ACKNOWLEDGEMENTS
We thank Inés Sanchez and Pedro Gomez de Nova for their help in the
laboratory of the IREC. We also are very grateful to the game managers for permission
to work in their hunting lands. This project was financed by CYCIT project CGL2004-
06147-CO2/BOS, by JCCM project PAC06-0137-2179, and the JCCM (F. Casas) and
CSIC-I3P (M. Calero-Riestra) grant programmes. JT Garcia was supported by a CSIC-
I3P post-doctoral contract. This article benefited from comments and suggestions
provided by J. Pérez-Tris during the manuscript preparation.
128
Capítulo 4
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134
CAPÍTULO 5
Efecto de la actividad cinegética en el comportamiento y la

distribución espacial del avefría europea, chorlito dorado y sisón
común en el oeste de Francia: Importancia de los refugios de caza en
áreas agrícolas
Casas, F., Mougeot, F., Viñuela, J. & Bretagnolle, V. Effects of hunting on the
behaviour and spatial distribution of northern lapwings, golden plovers and little
bustards in Western France: Importance of hunting-free refuges in agricultural areas.
Journal of Applied Ecology, en evaluación.
Capítulo 5
ABSTRACT
1. The increase in human leisure activities has amplified the potential

consequences of human disturbances on wildlife. Hunting is one of human
activities that affect most wildlife, and it has received increasing attention given
its social and economic dimensions. Most studies have been conducted on
coastal and wetland areas. Hunting activity can affect bird behaviour and
distribution and have a fitness cost. Hunting-free reserves for game species are
zones where birds find an area of reduced disturbance.
2. Our aim here is to evaluate the effect of hunting activities on the behaviour and
the use of hunting-free areas of lapwings, golden plovers and little bustards. The
first two species are hunted in France although showing less interest to hunters,
while the little bustard is fully protected since 1972. Also these birds inhabit
agricultural areas that are of conservation concern. We compared the use of
hunting free areas and the behaviour (time spent flying, vigilant, resting or
foraging) of birds on days before, during and after hunting took place. We took
into account variation due to time of day, date and group size. We also
monitored the hunting effect on the migration pattern on little bustard.
3. All three studied species showed behavioural responses to hunting activities.
After controlling for variations in behaviour due to time of day, date and group
size, we show that, in all studied species, hunting activity increased flight
probability and time spent vigilant (higher on hunting days than just before and
after a hunting day), to the detriment of resting. This implies greater energetic
costs on hunting days.
4. We also found distributional (use of hunting-free reserve) responses to hunting
activities. Little bustard almost never left the hunting reserves. Lapwings and
golden plovers used the hunting reserves mostly when hunting activity took
place and other areas when no hunting was conducted. Departures of little
bustards towards their wintering quarters could to be associated with the
occurrence of hunting.
5. Synthesis and applications. Hunting-free reserves appear to play a crucial role
for the management of game species and for the conservation of threatened
species in agricultural areas. Increasing the size or number of hunting-free areas
might be an important management and conservation tool to reduce the impacts
of hunting activities. An important measure to reduce hunting effect on little
bustard migration pattern could be to delay hunting until birds have left the area.
Management planning should also be integrated internationally for the creation
of refuge networks.
INTRODUCTION
Animals can perceive humans as potential predators and often alter their
behaviour in the presence of people. The increase in human population and leisure
activities has amplified the potential consequences of human disturbances on wildlife
(Blanc et al. 2006), including wild birds (Stockweel et al. 1991; Madsen & Fox 1995;
Fox & Madsen 1997; Bautista et al. 2005; Arroyo & Razin 2006; Holmes et al. 2006).
However, the overall effects of increasing human disturbance on bird populations are
137
still poorly documented (Guillemain et al. 2007), and there is often much debate about
how human activities must be regulated (see e.g. González et al. 2007, and references
therein). Several studies (including experimental ones) have shown that birds behave
differently in areas with contrasted levels of human disturbance (Fox & Madsen 1997;
Webb & Blumstein 2005), and that their avoidance behaviour may vary both temporally
and spatially, depending on the availability of alternative habitat and the fitness costs of
disturbance (Gill et al. 2001). Because all species do not respond with similar intensity
to human disturbances (Blumstein et al. 2005), it is important to take into account the
type of disturbance, their frequency, how, when and where they impact most on species
in order to adopt appropriate management measures aimed at reducing the negative
impact of human activities on wildlife.
Hunting is perhaps the human activity that affects wildlife most, and it has
received increasing attention given its environmental, social and economic dimensions,
particularly in Europe (Lucio & Purroy 1992, Martínez et al. 2002). Hunting is a
widespread human activity, with two complementary components that directly influence
the population dynamics of species: mortality and disturbance (Tamisier et al. 2003;
Pauli & Buskirk 2007), and is considered one of the main factor behind population
declines or extinctions of many species (Newton 1998). Hunting activity can however
be compatible with a conservationist policy, promoting and financing preservation of
natural ecosystems, in a context of “wise use”, whenever an adequate management plan
is implemented, adjusting human traditional activities, hunting and wildlife
conservation (Lucio & Purroy 1992; Tapper 1999; Robinson & Bennett 2004).
Most studies about the effect of hunting disturbance on birds have been
conducted on coastal, wetland, and forest birds, mainly focusing on waterfowl and game
species, and on effects on behaviour, distribution, abundance, and fitness of target game
species (Madsen & Fox 1995; Fox & Madsen 1997; Bregnballe et al. 2004; Duriez et al.
2005; Klaassen et al. 2006; Stafford et al. 2007; Thiel et al. 2007; Thiollay 2007).
These studies have evidenced that hunting causes local disturbance effects on target
game species, and may also affect other species of conservation concern (Madsen &
Fox 1995; Fox & Madsen 1997; Madsen 1998b). However, the effects that hunting and
game management have on non-target protected species are still poorly known (Arroyo
& Beja 2002). In a recent attempt to reduce hunting impact on behaviour and
distribution of wildlife, hunting reserves where birds can benefit from reduced
disturbance have been created in North America and in several European countries (e.g.
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Capítulo 5
Madsen 1998a; Madsen 1998b; Stafford et al. 2007), but their efficiency as
management tools has been poorly investigated yet (Duriez et al. 2005). Refuge size,
location and network structure must ensure birds find all their biological requirements,
reducing to a minimum the external disturbance (Fox & Madsen 1997).
Hunting activity is widespread in farmlands and agricultural habitats (Howard &
Carroll 2001; Martínez et al. 2002), but the effects of hunting on birds in these habitats
remains little studied as compared with birds inhabiting other habitats. This is important
because population declines have been reported in many bird species in agricultural
habitats (Donald et al. 2001; Robinson & Sutherland 2002). Farmland habitats (agrarian
pseudo-steppes) are under increasing pressure because of rapid natural habitat loss,
agricultural intensification and changes in land use (Bota et al. 2005). Thus, there is a
need for further research on the effects of hunting activities on key farmland bird
species, and on practical methods to reduce the effects that hunting activities might have
on species of conservation concern (Tucker & Heath 1994). Game shooting is one of the
main alternative options available to farmers in several European countries such as
France, Spain or the U.K. This activity often provides an added socioeconomic value in
some rural areas (Bernabeu 2000; Howard & Carroll 2001; Martínez et al. 2002).
Hence, hunting management programs should aim to enhance the conservation of game
birds together with that of the species that share the same habitat and ecological
requirements, and should be integrated with agricultural management programs (e.g.
Jolivet et al. 2007). In France, hunters of approximately one third of the 55,000
administrative districts (“Communes”), most of these in agricultural areas, are organised
into local associations (“Associations Communales de Chasse Agrée” or ACCA) that
manage hunting activities since 1991. In all ACCAs, at least 10% of the surface of the
Commune is set as a hunting-free reserve. All these are subject to common rules, in
most cases hunting is carried out only some days a week, and hunting is completely
prohibited inside these hunting reserves (Trouvilliez 1997).
Our aim here is to evaluate the effect of hunting activities on the behaviour and
the use of hunting-free areas of birds that inhabits agricultural areas in Western France,
and that are of conservation concern. These species are the northern lapwing (Vanellus
vanellus; hereafter “lapwing”), the european golden plover (Pluvialis apricaria;
hereafter “golden plover”) and the little bustard (Tetrax tetrax). The two former are
hunted in France, while the little bustard is fully protected since 1972. In western
France, farmland habitats hold c. 80 % of the country’s population of little bustards
139
(Jolivet et al. 2007), a threatened species, which confers international responsibility to

protect this population. We compared the use of hunting free areas and the behaviour
(time spent flying, vigilant, resting or foraging) of birds on days before hunting took
place, during a hunting day, and after a day of hunting. Behaviours might differ
depending on the time of day, date and group size (for instance, time spent in vigilance
is expected to decrease with increasing group size; McNamara & Houston 1992, but see
Beauchamp 2001), so we first investigated the effect of these factors on bird behaviour,
and then the effect of hunting. We predicted that birds would be more often disturbed
during hunting days, and would spend more time flying and being vigilant, to the
detriment of resting or foraging activities. We also predicted that birds would avoid
areas where disturbance due to hunting activities take place, and use more often
hunting-free areas when hunting takes place. Hunting activities may affect migratory
decisions (e.g. Béchet et al. 2003). We also investigated whether departures on
migration of little bustards coincided with hunting disturbances
Study Area
We conducted this study in a 340 km² cultivated area in South-Western France

(46°37’N, 0°2’W; Fig. 1) in October and November 2003. The habitat within the study
area is dominated by intensive agriculture with a mixture of winter cereal (c.50%), rape-
seeds (c.15%), sun-flower and maize (c.15%), with pasture and alfalfa being reduced to
less than 15%. Within this area, we studied more intensively a much smaller area (c. 10
km2) located between the villages of Tauché and Sainte-Blandine (“Commune” of
Tauché), hereafter referred as to the core study area (Fig. 1). In 2003, hunting season
was legally opened on 5 of October. In this ACCA, hunting was conducted twice a
week (on Thursdays and Sundays), by a variable number of hunters, from sunrise to
sunset, generally with a break in the middle of the day. Hunters locally targeted small
game mammals (european hares Lepus europaeus and wild rabbits Oryctolagus
cuniculus) and game birds (grey partridge Perdix perdix, red-legged partridge Alectoris
rufa and ring-necked pheasants Phasianus colchicus), showing less interest to lapwings
and plovers. Releases of captive bred partridges and pheasants are a common
management tool. The hunting method used was walk-up shooting with dogs (usually
140
Capítulo 5
one or two dogs per hunter, but sometimes up to six), the hunters forming an attacking
line of 3-6 hunters, spaced every c. 40-50 metres. Within the study area, hunting is
permitted in some areas, but not in other, which act as wildlife reserves (ACCAs) and
are most often located near villages (see Fig. 1). These are set by local hunters.
Tauché
1 km
Sainte-Blandine
Figure 1. Location and map of the study area in Western France (commune of Tauché). In white fields
outside the reserve, in grey hunting-free area. Black lines are tracks or roads used during transects. The
dots show the locations of lapwing and golden plover mixed flocks during non-hunting days (black dots
●) and during hunting days (white dots ○).
Study species
The lapwing is a medium-size wader with a widespread palearctic distribution.

Lapwings inhabit mainly grasslands and wet farmlands, where they feed on earthworms,
insects and others invertebrates, captured underground or over soil surface (Shrubb
2007). Lapwings winter commonly on the study area, most birds arriving in October-
November. The golden plover is a medium-size wader wintering on the coast or inland,
in pasture and arable farmland habitats throughout temperate south-western Europe
(Cramp & Simmons 1983). Golden plovers are less common than lapwings in our study
141
area, and typically form mixed flocks with lapwings. The little bustard is a medium-
sized Otididae typical of steppic and extensive agricultural habitats. In western France,
the species is migratory, birds leaving in early autumn towards their wintering quarters
in Spain (Morales et al. 2002). The little bustard breeding populations of western France
have suffered dramatic declines in recent years (Morales et al. 2005; Jolivet et al. 2007).
This species is currently classified as “Near Threatened” at the world level (BirdLife
2000), “Vulnerable” in Europe (Goriup 1994) and red-listed in France (Rocamora &
Yeatman-Berthelot 1999).
Data collection
Distribution, flock size and habitat use
We studied the distribution of focal species using road transects within the core
area. We regularly (every 1-2 days) and systematically looked for and mapped
individuals or flocks of the study species using always the same network of roads or
tracks, but in a different order every working day (Fig. 1). The high density of transects
within the study area gave us confidence of surveying correctly all the study zone and
detecting at least all flocks and most of isolated individuals of the focal species. The
observer was driving at low speed (20 km/h) and stopping regularly to look for, identify
and count birds using binoculars or a telescope. Observations were made from a
distance such that birds were not disturbed during transects. For each observation, we
recorded the date, time, exact location on a map, number of individuals of each species,
and the habitat used.
Transects were conducted before the start of the hunting season in the core area,
and on days before, during and after hunting took place. We began conducting transects
every working day from sunrise until 11.00 (am) and between 16.00 until sunset (pm).
Transects were not conducted in the middle of the day, when birds were less active,
following a bi-modal activity pattern commonly found in birds (pers. obs.; see Cope
2003; Roth & Lima 2007 and references therein), and when hunters use to have a break.
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Capítulo 5
Behavioural observations
When a flock was located, we randomly selected one individual within the flock,
and conducted a 60 sec (± 1) focal sampling (see Altmann 1974), using stop-watch and
a tape recorder. Observations were conducted from the car, which served as a hide, and
birds always seemed unconcerned by the presence of the observer. After each focal
sampling, we waited for 1-2 minutes before starting another focal sampling on another
bird. Birds were not individually marked, but we tried to sample individuals only once,
by switching to another bird that was at least at 10 metres from the previous focal one,
and only when we were confident that it was a different individual. The maximum
number of observation in a given flock was 20, 26 and 22, respectively for little bustard,
lapwing and golden plover.
Recordings of behavioural observations were subsequently analysed to quantify
the duration of each behaviour, which were defined and classified using prior
experience and previous works describing the main behaviours of study species
(Barnard et al. 1982; Cramp & Simmons 1980, 1983). Specifically, we recorded (1) the
occurrence of flight by the focal bird; (2) vigilance, recorded as the % time the focal
bird spent vigilant when landed; vigilant birds adopt a conspicuous upright body
posture, with the body, neck and head raised; (3) resting, recorded as the % time spent
resting or preening when landed; (4) foraging, recorded as the % time spent searching
for food (scanning, trampling) or feeding when landed. Lapwings and golden plovers
are “pause-travel” foragers, which mainly forage by scanning the area in front of them
and pecking at the substrate surface when prey is detected in a stop-run-stop fashion
(Barbosa 1995; Barbosa & Moreno 1999). Little bustard eat vegetation in winter, and
peck leaves while walking (pers. obs.).
For each observation, we also recorded the following data: sampling date (julian
date; 1= 1st of October), time of day, subsequently allocated to one of two daytime
period (am, 9.00-12.00 or pm, 16.00-19.00) and flock size (number of birds in the
group). Sample sizes for individual behavioural observations were as follows (n of
individual focal samplings): little bustard: n = 298; lapwing: n = 375; golden plover: n =
172.
143
Statistical analysis
Effects of hunting on behaviour
The probability of a bird flying during a watch was fitted to models using a
binomial error distribution and a logit function. The % time spent by focal birds in
different behaviour (arcin transformed) was fitted to models using a normal error
distribution and an identity link function. Explanatory variables included the daytime
period (am vs pm), the sampling date (julian date), the group size and the hunting
activity (three classes: day before hunting, day when hunting took place, day after
hunting). We tested for non-linear relationships with sampling date or group size by
including a quadratic term in the model (date2; group size2), and kept it in our models
when significant (P < 0.05). When variation in behaviour was explained by hunting
activity, we conducted pairwise comparisons between days before, during and after
hunting took place.
Effects of hunting on spatial distribution
To investigate differences in the use of the hunting reserve depending on hunting

activity by little bustards or mixed flocks of lapwing and golden plover (day before
hunting day, hunting day and day after hunting), we performed a Chi-square analysis on
a contingency table with the variables “reserve use” and “hunting day”.
We fitted the variable “reserve use” to the model using a binomial logistic model
with log link function. To control for variations due to daytime period, date, habitat,
flock size and hunting activity (before hunting day, hunting day and after hunting day)
we included these as explanatory variables in the models. The significance of the effects
was tested using the Wald statistic (test of significance of the regression coefficient).
144
Capítulo 5
Table 1. Effects of daytime period, date, group size and hunting activity on the behaviour of studied species. Only the final models are presented. All initial models included
daytime period (am vs pm), sampling date and sampling date2, group size and group size2 (to test for linear or quadratic relationships with date or group size) and hunting
activity (day before, during or after hunting took place). Non-significant variables (P = 0.10 level) were removed sequentially using a backward selection procedure.
Behaviour Source of variation Little Bustard Northern Lapwing Golden Plover

df Chi2 P df Chi2 P df Chi2 P
Flying probability Daytime period 1,290 9.57 0.039 1,367 4.22 0.039 1,166 11.32 <0.001
Group size 1,367 6.08 0.014
Group size2 1,367 16.72 <0.001
Hunting activity 2,290 6.15 <0.001 2,367 34.53 <0.001 2,156 15.46 <0.001
df F P df F P df F P
Vigilance Daytime period 1,283 5.53 0.019 1,266 5.04 0.026
Date 1,283 6.70 0.010 1,266 4.11 0.044
Date2 1,283 6.91 0.009
Group size 1,283 3.49 0.063 1,266 4.93 0.027
Hunting activity 2,283 19.54 <0.001 2,266 9.93 <0.001 2,107 9.26 <0.001
Resting Daytime period
Group size 1,283 4.57 0.033 1,266 6.66 0.010
Group size2 1,283 6.34 0.012
Hunting activity 2,283 8.45 <0.001 1,266 3.19 0.043 2,107 6.57 0.002
Foraging Daytime period 1,266 5.04 0.026
Date 1,266 7.70 0.006
Group size 1,283 15.37 <0.001
Group size2 1,283 16.96 <0.001
Hunting activity 2,283 0.37 0.693 1,266 1.24 0.290 2,107 0.38 0.684
145
RESULTS
Hunting and behaviour
Flying
Variation in the occurrence of flights by little bustards was not significantly

explained by sampling date or flock size but was explained by daytime period (flights
were observed only am) and hunting activity (flights were observed only on hunting
days; Table 1; Fig. 2).
For lapwings, flight probability during a watch was not significantly explained
by sampling date, but was explained by daytime period (birds were more likely to fly
pm than am), flock size (quadratic function: flight occurrence decreased with increasing
group size, but increased in larger groups, ie. > 500 individuals) and hunting activity
(Table 1; Fig. 2). Lapwings were more likely to fly on hunting days than on days prior
to hunting (F1, 233 = 33.09; P < 0.001) or after hunting (F1, 250 = 6.73; P = 0.009), and
were also more likely to fly on days after hunting than on days before hunting (F1, 250 =
14.61; P = 0.001).
For golden plovers, variation in flight probability was not significantly explained
by sampling date or flock size, but was explained by daytime period (birds were more
likely to fly am than pm) and hunting activity (Table 1; Fig. 2). Golden plovers were
more likely to fly on hunting days than on days prior to hunting (F1, 92 = 9.46; P =
0.002), but not on days after hunting as compared with hunting days (F1, 113 = 0.47; P =
0.495). Flying probability was significantly higher on days after hunting than on days
before hunting (F1, 130 = 12.16; P < 0.001).
Time spent vigilant.
Variation in the % time spent vigilant by little bustards was explained by

daytime period (birds spent more time vigilant am than pm), sampling date (vigilance
increased non-lineraly, peaking at the end of the study period), flock size (vigilance
tended to decrease linearly with increasing group size) and by hunting activity (Table 1;
Fig. 2). Little bustards spent more time vigilant on hunting days than on days prior to
hunting (F1, 169 = 16.77; P < 0.001) or after hunting (F1, 203 = 29.85; P < 0.001). Time
146
Capítulo 5
spent vigilant did not differ significantly between days before or after hunting (F1, 190 =
0.27; P = 0.607).
For lapwings, variation in the % time spent vigilant by lapwings was explained
by daytime period (birds spent more time vigilant pm than am), sampling date (time
spent vigilant increased linearly with date), flock size (vigilance decrease linearly with
increasing group size) and by hunting activity (Table 1; Fig. 2). Lapwings spent more
time vigilant on hunting days than on days prior to hunting (F1, 172 = 16.37; P < 0.001)
or after hunting (F1, 166 = 14.12; P < 0.001), but time spent vigilant did not differ
significantly between days before or after hunting (F1, 191 = 2.86; P = 0.087).
For golden plovers, variation in the % time spent vigilant was not significantly
explained by daytime period, sampling date or flock size, but was explained by hunting
activity (Table 1; Fig. 2). Golden plovers spent more time vigilant on hunting days than
on days prior to hunting (F1, 67 = 19.87; P < 0.001) or after hunting (F1, 66 = 4.25; P =
0.043), and also spent more time vigilant on days after hunting than on days before
hunting (F1, 87 = 8.87; P = 0.004).
Time spent resting.
Variation in the % time spent resting by little bustards was not significantly
explained by daytime period or sampling date, but was significantly explained by flock
size (quadratic relationship: resting increased with increasing group size, but decreased
for largest groups) and by hunting activity (Table 1; Fig. 2). Little bustards spent less
time resting during a hunting day than on a day before hunting (F1, 169 = 10.55; P =
0.001) or after hunting (F1, 203 = 16.74; P < 0.001), but spent a similar amount of time
resting on days before and after hunting (F1, 190 = 0.08; P = 0.772).
For lapwings, variation in the % time spent resting was not significantly
explained by daytime period or sampling date, but was significantly explained by flock
size (resting increasing linearly with increasing group size) and by hunting activity
(Table 1; Fig. 2). Lapwings spent less time resting during a hunting day than on a day
before hunting (F1, 174 = 6.98; P = 0.009) or after hunting (F1, 168 = 5.22; P = 0.024), but
spent a similar amount of time resting on days before and after hunting (F1, 193 = 0.22; P
= 0.643).
For golden plovers, variation in the % time spent resting was not significantly
explained by daytime period, sampling date, or flock size, but was explained by hunting
147
activity (Table 1; Fig. 2). Golden plovers spent less time resting during a hunting day
than on a day before hunting (F1, 67 = 9.11; P = 0.004) or after hunting (F1, 66 = 55.65; P
= 0.020), but spent a similar amount of time resting on days before and after hunting
(F1, 87 = 0.92; P = 0.339).
After hunting
Before hunting
Hunting day
Little bustard Lapwing Golden plover

0.10 0.6 0.6
0.5 0.5
0.08
0.4 0.4
0.06
Flight
0.3 0.3
0.04
0.2 0.2
0.02 0.1 0.1
0.00 0.0 0.0

50
60 60
40
Vigilance
30 40 40
20
20 20
10
0 0 0
50
50 50
40
40 40
Resting
30
30 30
20
20 20
10 10 10
0 0 0
40
25 30
30
20
Foraging
20
20 15
10
10
10
5
0 0 0
Figure 2. Mean ± SE flight probability and time spent vigilant, resting and foraging by little bustards,
lapwings and golden plover according to hunting activity (before a hunting day, when hunting took place
and after a hunting day).
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Capítulo 5
Time spent foraging.
Variation in the time spent foraging by little bustards was not significantly
explained by daytime period, sampling date or hunting activity (Table 1; Fig. 2) but was
explained by flock size (quadratic function; time spent foraging increased with
increasing group size, but decreased in largest groups; Table 1).
For lapwings, variation in the time spent foraging was explained by daytime
period (lapwing spent more time foraging am than pm) and sampling date (time spent
foraging decreased with date), but was not significantly explained by flock size or
hunting activity (Table 1; Fig. 2).
For golden plovers, variation in the time spent foraging was not significantly
explained by daytime period, sampling date, flock size or hunting activity (Table 1; Fig.
2).
120 Before Hunting

Hunting Day
% of observations within hunting-free area
8 8 After Hunting
100 22
12
80
60
40
17 17
20
0
little bustard lapwing and golden plover mixed flocks
Figure 3. Use of hunting-free reserves (% of observations) by mixed flocks (lapwing and golden plover)
and by little bustards according to hunting activity: before a hunting day (white bars), when hunting took
place (stripped bars) and after a hunting day (black bars). Sample size refers to number of flocks.
Hunting and use of hunting-free reserves
We found significant differences in the use of hunting reserves before, during

and after a hunting day by lapwing and golden plover mixed flocks (χ² = 23.581, df = 2;
149
P < 0.001). Flocks were more often found within hunting reserves when hunting took
place than when it did not (Wald = 12.234; P = 0.0022; Fig. 3). Variation in the
probability of using the reserve was not explained by flock size (Wald = 0.053; P =
0.81), daytime period (Wald = 0.17; P = 0.67), sampling date (Wald = 0.846; P = 0.35)
or habitat (Wald = 2.476; P = 0.47), nor by any of the interactions between these
variables.
Little bustards almost exclusively used the hunting-free area. All but one of the
observations of little bustards (n = 26) was outside the hunting reserve (Fig. 3).
Hunting and migration departures of little bustard
We found that the first and last departures of little bustards towards their
wintering quarters were associated with the occurrence of hunting. The main departure
(c. 60% of the little bustards present in the area) was observed just after the first hunting
day (Fig. 4). Birds that remained in the area late in the season were mainly young birds
released as part of a restocking program to reinforce declining populations in western
France.
90
POPULATION SIZE
80 HUNTING DAY
70
60
Population Size
50
40
30
20
10
0
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26
Date
Figure 4. Seasonal variations (day 1 = 1 October 2003) in the number of little bustard counted on the
study area.
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DISCUSSION
We found that all three studied species showed behavioural as well as

distributional responses to hunting activities, after considering other possible sources of
variations factors, such as flock size, time of day, or date. The effects of the latter varied
depending on the species, while the effect of hunting disturbance was fairly consistent
across species. This is in accordance with the hypothesis that, if hunting is a relevant
disrupting source, birds would be more often disturbed during hunting days, and would
avoid areas with disturbances due to hunting activities and use more often hunting-free
areas. Because we found similar behavioural effects of hunting activity in northern
lapwing, golden plover and little bustard, hunting might similarly affect other birds
occupying the same habitat, highlighting potential implications at a community level.
Disturbance associated with hunting activity reduced the time spent by birds resting but
increased the time spent being vigilant and flying. However, we found no evidence that
it affected the time spent feeding or foraging. These results are similar to those found in
other species (Riddington et al. 1996; Madsen 1998a; Madsen 1998b; Féret et al. 2003).
Hunting activity affected behaviour, distribution and migration pattern, revealing that
this activity causes disturbance and may induce additional energetic costs (Jarvis 2005).
Factors other than hunting affecting variation in behaviour
Little bustard flights were exclusively observed in the morning, when they also
spent more time vigilant. Clear daily rhythms in activity patterns were also found for
lapwings, which were observed flying more frequently and spending more time vigilant
in the afternoon, while they spent more time foraging in the morning. Time devoted to
vigilance and flights may reflect predation risk, and be related to predators´ daily
activity rhythms (Roth & Lima 2007). In the case of golden plovers, we only found an
effect of time of day on flight frequency, higher in the morning. These differences
between two species gathering in common flocks may be related to their contrasted
foraging ecology (see Gillings et al. 2005).
We found few significant effects of sampling date on behaviour, something that
could be expected given the relatively short study period (two months). We found that
little bustards and lapwings increased time devoted to vigilance during the study period.
This could be a consequence of the start of hunting season, given the effects of hunting
151
on vigilance, and would indicate, at least for little bustards, that birds might not
habituate to hunting disturbance. This could also be because time spent vigilant
decreased with group size, and group size decreased as birds departed on migration. For
lapwings, other factors not considered in this study, such as new arrivals and a high
turnover of wintering birds, could also explain this increase in vigilance. In lapwings,
time spent vigilant increased linearly with date, while time spent foraging decreased
over the same period, suggesting a trade-off between these two activities. These inverse
patterns may be related with higher energy demand just after first arrivals of migrants at
the beginning of the autumn season that progressively decrease as they settle in the area,
or an increase in foraging proficiency as they become acquainted with food resources in
wintering grounds.
Flock size had an important effect on the time spent foraging and resting in the
little bustard, both increasing with group size, but decreasing in largest groups, which
may be explained by scramble competition (Beauchamp 2001). When resources are
limited, a reduction in vigilance may allow individuals to spend more time foraging and
thereby obtain a greater share of the resources available to the group (Beauchamp &
Ruxton 2003). However, under intraspecific competition, individuals might spend more
time vigilant in larger groups to avoid displacement by aggressive individuals (Treves
2000) or to locate the food discovered by other individuals (Beauchamp 2001), which
may reduce the time spent foraging. In our case, competition for a limited food resource
is plausible, because just before departing on migration, little bustards need to increase
their energetic storage (fat and protein) and food resources can be temporally limited.
Lapwings and golden plovers are considered as “pause-travel” foragers (Barbosa
& Moreno 1999), so flock size should not influence the scan rate behaviour (Barbosa
2002). In golden plovers, flock size did not influence at all behaviour. In lapwings,
however, time spent vigilant decreased with group size, while resting increased. In this
species, flocking thus seem to decrease the proportion of time that each individual
spend vigilant (Redpath 1988), allowing birds to spend more time in other activities,
like resting. The lack of such an effect in golden plovers could be due to feeding
interference when there were large numbers of lapwings relative to plovers (Barnard et
al. 1982). Golden plovers may also benefit from Lapwings vigilance in mixed-species
flocks.
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Hunting disturbance and behaviour
Hunting disturbance caused increased flight frequency and time spent vigilant, to
the detriment of resting. These behavioural effects were consistently found in the three
studied species. Flying more often and spending more time vigilant to the detriment of
resting implies greater energetic costs, and in some cases may lead to a greater
predation risk (e.g. Béchet et al. 2004; Jarvis 2005). Lapwings and golden plovers also
spent more time flying after a hunting day, indicating that the disturbance effects may
last at least for a day after the hunting activity had ceased. This effect might be the sum
of a behavioural and distributional change caused by hunting disturbance, since birds
used hunting-free reserves mainly on hunting days and the area around reserve on other
days (see below). Little bustards and lapwings recovered quickly after a hunting day
their basal time spent vigilant. However, golden plovers remained more vigilant after a
hunting day, suggesting that they might be less tolerant and particularly sensitive to this
type of disturbance.
In order to save energy, birds usually resort to resting. In migratory species, like
little bustards, fat storage might be particularly important prior to the migration (Féret et
al. 2003; Berthold 2002). Fat storage rates can be affected by intrinsic (as shedding
timing or corporal mass) or extrinsic factors (food availability or predation risk;
Berthold 2002). Hunting disturbance might reduce nutrient storage by increasing time
spent flying or vigilant (Féret et al. 2003; Béchet et al. 2004). We did not find that time
spent foraging decreased with hunting activity, but flight probability increased on
hunting days, which implies a higher energy consumption. The time spent foraging by
lapwings and golden plovers were lower than for little bustard, may be because they are
more nocturnal feeders than little bustards. Little bustards are herbivorous in autumn
and winter (Cramps & Simmons 1980), and this food source is relatively poor (low rates
of energy assimilation per unit of mass consumed). Bustards may thus need to forage
more during the day than invertebrate feeders, such as shorebirds, which can
complement their food supply needs at night (Gillings et al. 2005).
Hunting activity and use of hunting-free reserves
Little bustards almost never left the hunting reserves during hunting season, and
may be thus particularly sensitive to this kind of disturbance. Hunting-free reserves thus
153
appeared crucial for this endangered species. In contrast, lapwings and golden plovers
used the hunting reserves mostly when hunting activity took place, but quickly resumed
using other areas as soon as hunting stopped. Therefore, a game management plan based
on reducing the number of hunting days per week (like the one implemented in many
rural ACCAs in France) could be enough to minimize the impact of hunting disturbance
on some species, but not in others. Madsen (1998b) did not find a preferential use of
hunting-free reserves by lapwings and golden plovers, but his study focused on
migratory waterfowl, and was thus designed to study primarily the usefulness of hunting
reserves in wetlands for waterbirds (protected areas had limited shore and did not
include adjacent terrestrial habitats, which may be more important for wintering
lapwings and plovers than shores). In fact, when including adjacent terrestrial habitats
into the hunting-free reserves for waterfowl, golden plovers and lapwings moved to
non-hunted areas as a quick response to start of hunting activity (Bregnballe & Madsen
2004).
Our findings are consistent with those previous work conducted mainly on
wetland and forest game species (e,g, Ebbinge 1991; Percival et al. 1997; Béchet et al.
2004; Bregnballe & Madsen 2004; Duriez et al. 2005). They highlight that hunting-free
reserves play a crucial role for the management of game species as well as for the
conservation of threatened ones, like little bustards. Furthermore, if reserves are
hunting-free all year round (like ACCAs in France), they could also benefit breeding
birds when hunting also occurs during breeding season.
Hunting and little bustard migration pattern
Hunting disturbance may not only influences habitat use, but also migration
patterns, as found in other birds subject to heavy hunting pressure such as waterfowl
(Fox & Madsen 1997; Percival et al. 1997; Béchet et al. 2003). As a response to hunting
activity, birds may migrate earlier, change migration routes or wintering areas. In
migratory little bustards, we found that the first main departure occurred just after the
first hunting day, suggesting that hunting may influence migration. Little bustards
migrate at night (Morales, M. and García de la Morena, E., unpublished data), and
hunting disturbance the previous day may have stimulated the departure decision.
However, more information would be needed to confirm these patterns.
154
Capítulo 5
With the necessary caution when dealing with results obtained at a local level,
our findings showed similar disturbance effects of hunting activity on three species that
share the same habitat (agricultural area) at the beginning of the hunting season. These
three species had different life histories and ecological requirements, suggesting that
hunting disturbance may affect a wide range of species. Our study showed that hunting
caused behavioural changes and displacement of birds from hunting areas to reserves
areas on hunting days. Thus, our results indicate that game reserves are an effective
management tool to mitigate the effect of hunting activities and promote conservation
of species of conservation concern in agricultural areas.
However, at least three caveats to that efficacy could be raised. First, some
species particularly sensitive to hunting disturbance could restrict themselves to game
reserves during hunting season. This was apparent for little bustards in our study.
Species confined within hunting-free reserves might have a reduced choice of feeding
habitats. For little bustards, crops such as rape-seed or alfalfa, are particularly important
for foraging at this time of year (pers.obs.; Wolff et al. 2001), probably because they
provide relatively high energy as compared with other available crops. Therefore,
habitat availability inside and outside the hunting reserves should be an important factor
to consider in the design of these reserves in areas within the range of this endangered
species.
Second, we detected some important differences in the level of sensitivity to
hunting disturbance, from complete confinement to hunting-free areas in the case of
little bustards, to movements in and out of reserves depending on hunting activities in
the case of golden plovers and lapwings. Studies on the effects of hunting disturbance
should be conducted a wider range of species to better understand the real impact of
hunting disturbance on the whole bird community (Gill et al. 2001).
Finally, birds often respond to disturbances as if it was a predatory event. Birds
can become habituated to their local level of disturbance, becoming more tolerant in
more disturbed areas (Blumstein et al. 2005) which could make them more susceptible
to predation (Webb & Blumstein 2005). Game reserves considered in this study were of
recent creation (1991), and it could be useful to replicate this kind of study in areas
where reserves have been established for longer periods.
155
Hunting activity encompasses disturbances by pedestrian (hunters), dogs and

gunshots, which are difficult to separate from each other, since they all occur
simultaneously. Mobile hunting techniques generally cause greater disturbance than
hunting from a fixed point (Fox & Madsen 1997). Additionally, when hunters go with
dogs, there is a further source of disturbance, given the predatory and searching
behaviour of dogs (Martinetto et al. 1998; Lafferty 2001). The way hunting is
conducted may thus be adapted to minimize disturbance effects.
An increase in the size of hunting-free areas might mitigate hunting disturbance,
and could be an important management tool. This could be particularly important in
areas where threatened species as little bustard are present, due their dramatic
population declines in recent years (Morales et al. 2005; Jolivet et al. 2007). In such
cases, another alternative might be the payment of incentives to hunters for increasing
the size of the hunting-free areas. In any case, if an increase of hunting-free areas is
applied as a hunting disturbance buffer, it is important to identify minimum size and
threshold levels of disturbance that can to be compatible for hunting activity and
conservation. The possible effect of hunting on the autumn migration departures of little
bustards could be mitigated by delaying the start of hunting until most birds have left
the area. Management planning should also be integrated internationally, especially for
migratory species by creating a network of refuges. This could be particularly important
in the centre-south of Spain, the main wintering area for little bustards of western
France population (Morales et al. 2002).
ACKNOWLEDGMENTS
For this work FC was supported by a Marie Curie fellowship of the European
Community programme. He thanks the students and researchers at Chizé station during
his stay for field work, which helped him to do more bearable that time, especially to
Carole Attié, Loïc Hardouin, Alex Millon and Diane Desmonts. FM was supported by a
NERC advanced fellowship, a Grant from the Spanish Ministerio de Educacion y
Ciencia, Spain (CGL 2006-11823) and from the Junta de Communidades de Castilla-
La-Mancha, Spain (PAI06-0112). FM was supported by a NERC advanced fellowship,
a Grant from the Ministerio de Educación y Ciencia, Spain (CGL 2006-11823) and
from the JCCM, Spain (PAI06-0112).
156
Capítulo 5
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SÍNTESIS
Síntesis
SÍNTESIS: PERSPECTIVAS DE INVESTIGACIÓN FUTURA Y

APLICACIONES DE GESTIÓN.
La caza en España, lejos de constituir una actividad necesaria para la

supervivencia, sigue siendo sin embargo una de las actividades lúdicas que mayor
interés despierta, tanto desde el punto de vista económico como social. Por tanto,
conocer los factores que pueden influir en la dinámica poblacional de la principal ave de
interés cinegético de la península Ibérica, así como cuales pueden ser las mejores
estrategias de gestión agrícola y cinegética, junto con los efectos indirectos derivados,
tanto de la caza propiamente dicha, como de algunas de las herramientas de gestión más
utilizadas en los últimos años (suelta de perdices de granja), son un paso clave para
desarrollar estrategias de gestión efectivas. Por un lado, estas estrategias deberían
garantizar la estabilidad de las poblaciones silvestres de perdiz roja, y por otro, la
conservación de su hábitat, lo cual puede beneficiar a otras especies con las que ésta
comparte el espacio. Esta tesis ha tratado de avanzar en ese sentido, pretendiendo trazar
unas futuras líneas de actuación en las que tanto el aprovechamiento cinegético como
agrícola sean compatibles con la conservación del medio y, en consecuencia, de las
especies que lo habitan.
Parámetros reproductivos: Nuevos resultados
Antes de desarrollar cualquier tipo de estrategia de gestión para una determinada

especie, es importante conocer cuales son los principales puntos donde uno debe incidir.
Para ello, como paso inicial es primordial conocer a fondo la ecología reproductiva de
esa especie. Al igual que para otras especies, dada la conocida variabilidad interanual en
la cría de la perdiz roja (Lucio 1990; Rueda et al. 1993), se precisa información
detallada durante varios años, especialmente en aquel hábitat donde la perdiz roja
alcanza sus mayores densidades, la pseudoestepa agraria (Blanco-Aguiar et al. 2003).
Uno de los resultados más relevantes de este trabajo es haber constatado el
importante papel de los machos en la reproducción de esta especie. En el capítulo 1 de
esta tesis doctoral se muestra, por primera vez, el porcentaje de machos dentro de una
población que pueden hacerse cargo del cuidado de una puesta. Aunque el hecho de que
los machos incuben pudiera parecer un comportamiento anecdótico con interesantes
connotaciones evolutivas discutidas en dicho capítulo, en realidad su contribución a la
165
productividad de una población de perdices puede ser importante. Así pues, el

rendimiento cinegético de la temporada de caza siguiente fue menor el año que los
tamaños de puesta fueron menores y como consecuencia no incubaron los machos.
La regulación del tamaño de puesta, junto con el éxito de eclosión podrían ser
los principales rasgos determinantes de la frecuencia de aparición de este
comportamiento de doble puesta en una población (Green 1984; Fernández & Reboreda
2007). La hembra puede regular su inversión reproductiva en base a diferentes
parámetros, entre los que destacan el compromiso reproductivo de su pareja, el clima y
la disponibilidad de recursos del medio. Otros factores como la edad y la condición
física y, en particular, la densidad de población también pueden contribuir a explicar la
frecuencia de aparición de este comportamiento. Aunque nuestro trabajo ya recoge
datos de una cantidad considerable de años, serían necesarias series más largas,
protocolos experimentales, o muestreos simultáneos en diversas áreas de estudio, para
esclarecer cual es la importancia relativa del clima, la densidad o los depredadores sobre
la inversión de los machos en la incubación.
Nuestros datos apuntan al clima, como factor de especial importancia sobre los
parámetros reproductivos (fecha de inicio de puesta, frecuencia de dobles puestas y
tamaño de puesta), tal y como sugieren otros trabajos (Lucio 1990; Villanúa 2007). Sin
embargo, faltaría explorar en mayor profundidad el papel de la densidad de población y
el riesgo de depredación. La integración de toda esta información permitiría desarrollar
modelos demográficos para predecir las tendencias poblacionales en diferentes
circunstancias, que proporcionarían una herramienta de gestión vital de gran ayuda en la
toma de decisiones sobre la mejor estrategia de gestión aplicable en un momento dado.
En ese caso, faltaría añadir información acerca de las causas que puedan influir en la
regulación del número de pollos y su crecimiento hasta alcanzar la edad adulta, que es
otra de las piezas fundamentales para completar la información necesaria para el
desarrollo de modelos demográficos, recogiendo información de las diferentes fases del
ciclo de vida de la especie.
Para el gestor cinegético que basa sus futuras bolsas de caza en la productividad
y mejora de la supervivencia de la perdiz en el campo, puede ser muy útil disponer de
este tipo de información. Por un lado, la capacidad de las hembras para la producción de
huevos depende de los recursos del medio (Monaghan & Nager 1997; Lepage & Lloyd
2004) y está sujeta a fuertes variaciones interanuales (Cattadori et al. 1999; Watson et
al. 2000). A nivel de gestión, poco puede hacerse ante la variabilidad climática
166
Síntesis
interanual experimentada en ambientes mediterráneos (Blondel & Aronson 1999), pero

sí se podría actuar para reducir dicha variabilidad interanual en la disponibilidad de
recursos tróficos en el período más crítico de la reproducción. Dentro de nuestra área de
estudio, el aporte suplementario de alimento no fue una de las herramientas de gestión
utilizada. Sin embargo, y como señalamos en la Introducción de esta tesis, es una
herramienta de gestión frecuente (Díaz 2006), aunque se sabe muy poco sobre su efecto
en los parámetros reproductivos de la perdiz roja en el área mediterránea. Sí se conoce
sin embargo, que la alimentación suplementaria de perdices silvestres puede tener serias
consecuencias negativas sobre su fisiología y anatomía interna, que pueden conducir a
problemas de supervivencia en libertad (Millán et al. 2003). Por tanto, serían necesarias
futuras investigaciones para clarificar los efectos del aporte suplementario de alimento,
no solo en la ecología reproductiva, sino igualmente en la supervivencia y condición
física de la perdiz roja.
Por otro lado, una modalidad de aprovechamiento cinegético complementario
tras el cierre de la veda general en muchos cotos, es la caza de perdiz con reclamo. Esta
modalidad puede a su vez formar parte integral de la gestión cinegética, como de hecho
es frecuente. En tales casos, la caza con reclamo se usa como herramienta para reducir
el número de machos, bajo la creencia popular del efecto deletéreo de un hipotético
“exceso” de machos en el éxito de nidificación (los bandos de machos denominados
popularmente “toradas”, que se creé destruyen nidos de otras perdices). A la luz de
nuestros resultados, los machos abatidos mediante esta modalidad podrían ser aquellos
más agresivos, que posiblemente tengan menor tendencia a incubar puestas (Mougeot et
al. datos no publicados), y por tanto la caza con reclamo no tendría un gran efecto sobre
la población. Pero, por otro lado, puede que los considerados tan a menudo como
machos “sobrantes” sean en realidad piezas clave para aumentar la productividad global
de una población silvestre de perdiz roja. Urge profundizar en este tipo de aspectos en
relación con la caza de la perdiz con reclamo, ya que pueden ser clave para mejorar la
estrategia de gestión de sus poblaciones.
¿Gestión del hábitat o control de depredadores?
Como se comentaba en la Introducción de esta tesis doctoral, las poblaciones

naturales de perdiz roja sufrieron una marcada regresión en las últimas décadas, en
prácticamente toda su área de distribución. Diversas razones podrían explicar este
167
declive, pero la más importante parece ser la alteración del hábitat, particularmente en
los medios agrarios (Lucio & Purroy 1992, Blanco-Aguiar et al. 2003, 2004; Vargas et
al. 2006, Blanco-Aguiar 2007). Sin embargo, poco se sabe sobre cual de los múltiples
cambios que la modernización en los sistemas de explotación agraria ha producido en el
ecosistema puede explicar dicho declive. Según nuestros resultados, la desaparición de
las lindes como consecuencia de la intensificación agrícola (Pain & Pienkowski 1997;
Fuller 2000), junto al impacto negativo de las prácticas agrícolas (principalmente
cosecha) sobre el éxito de nidificación, pueden ser los dos factores directos más
importantes para explicar el declive generalizado de las poblaciones de perdiz roja. La
selección positiva de las lindes como sustrato de nidificación, junto con el mayor éxito
de nidificación de los nidos situados en estos hábitats, serían la causa próxima de la
mayor densidad de esta especie en zonas donde la superficie de este elemento del
paisaje agrícola es más abundante (Rands 1986; Peiró 1992; Lucio & Purroy 1992;
Blanco-Aguiar et al. 2003). Por otro lado, el fuerte efecto de la cosecha sobre el éxito de
nidificación de la perdiz, junto al efecto relativamente más débil de la depredación,
evidencian una vez más, especialmente en áreas agrarias, que la principal estrategia de
gestión para el mantenimiento de poblaciones silvestres saludables es la gestión del
hábitat (Rands 1987a,b; Duarte & Vargas 2002).
Nuestros resultados permiten acotar cuáles serían las estrategias aplicables más
importantes en cuanto a gestión agraria. Estas medidas principales serían el
mantenimiento y, en lo posible, un aumento de la superficie ocupada por las lindes y un
retraso en la fecha de cosecha (al menos en la franja de 5 metros más externa de las
parcelas de cereal). Estas acciones, unidas a la preservación del tradicional paisaje en
mosaico de los campos de cultivo, no sólo beneficiarían a las poblaciones de perdiz,
sino también a un gran número de especies que comparten su hábitat, especialmente
aquellas afectadas por la disminución de la superficie de las lindes (Tella et al. 1998;
Vickery et al. 2002; De la Concha et al. 2006) y las que pueden ser potencialmente
afectadas por la cosecha, como los aguiluchos (Circus sp.; Castaño 1995; Arroyo et al.
2002) o los sisones (Tetrax tetrax; Carole Attié, comunicación personal).
La comunidad cinegética a menudo considera la depredación como el principal
factor detrás de la reducción en el éxito reproductivo de las especies de caza menor
(Nadal & Comalrena 1994). Por ello, el control de depredadores es la herramienta de
gestión más utilizada (Arroyo & Beja 2002). Sin embargo, nuestros resultados indican
que al menos en lo que se refiere a la fase de puesta e incubación, la actuación sobre la
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Síntesis
gestión agraria sería una estrategia mucho más eficaz que el control de depredadores. Es
importante reseñar que esta baja importancia relativa de la depredación no parece
deberse a la gestión relacionada con el control de depredadores, al menos en nuestra
área de estudio. De hecho, hay notables diferencias en la intensidad del control de
depredadores entre los cotos estudiados, y en alguno de ellos la abundancia de
depredadores antropófilos (gatos y perros asilvestrados), los considerados más dañinos
para la perdiz roja, es relativamente alta. A pesar de ello, no encontramos diferencias
significativas ni en la tasa de pérdida de nidos ni en las causas de pérdida entre cotos.
Estos resultados podrían ser una pieza crucial de información para comenzar a
solucionar el conflicto entre gestión cinegética y conservación de la biodiversidad
(Valkama et al. 2005).
Efectos de las sueltas de perdices de granja
La suelta de perdices procedentes de granja se ha convertido en una de las

herramientas de gestión más extendidas, tanto a nivel nacional como internacional. Los
objetivos de los gestores que llevan a cabo este tipo de práctica son muy diferentes a los
perseguidos por los gestores de poblaciones de perdiz silvestre, y por tanto, los efectos
tanto en las propias poblaciones de perdices como en las poblaciones de otras especies
que habitan en la misma área, también podrían ser distintos.
Por un lado, la baja efectividad de las sueltas de aves procedentes de granjas ha
sido demostrada en varias especies (Leif 1994; Gortazar et al. 2000; Putaala & Hissa
2003), lo cual podría dar lugar a pensar que el riesgo potencial (transmisión de parásitos
e introgresión genética) sería muy reducido, ya que su período de permanencia en el
campo es relativamente bajo. Pero, por el contrario, se han ido acumulando evidencias
de los efectos negativos de estas sueltas, tanto sobre otras especies con las que
comparten el mismo hábitat como sobre las poblaciones silvestres de las propias
especies liberadas (Tompkins et al. 2001; Villanúa et al. 2007), principalmente debido a
la sobrecaza (Keane et al. 2005), la transmisión de parásitos (Villanúa et al. en prensa)
y la introgresión genética (Blanco-Aguiar 2007).
La sobrecaza no es sólo un efecto derivado de la sueltas de aves procedentes de
granja, sino que puede producirse en cualquier área donde que no marque un cupo de
capturas, sin tener en cuenta que las temporadas de caza venideras dependen de los
individuos que se dejen vivos para la siguiente temporada de cría, independientemente
169
de que se suelte perdiz o no. La perdiz roja es una especie muy sensible a la
sobreexplotación cinegética, quizás el mejor ejemplo es el desastre portugués durante la
conocida como revolución de los claveles (1974-1988). Durante ese período se
esquilmaron las poblaciones de perdices, puesto que la caza era libre y la única
limitación era un cupo de piezas por día (Martínez et al. 2002). A pesar de esto, tras la
aparición de la Ley de 1988 (promoción de acotados y caza sostenible), en 1996 el 30 %
del país estaba acotado, y en poco más de 3 años de protección la densidad de las
perdices se vio triplicada (Martínez et al. 2002). Por tanto, a pesar de esa sensibilidad a
la sobreexplotación, las poblaciones de perdiz tienen gran capacidad de recuperación.
De forma más general, la sobrecaza afecta a la viabilidad poblacional de muchas otras
galliformes (Keane et al. 2005).
En cuanto a la sobrecaza debido a las sueltas masivas de perdices rojas, en el
Reino Unido por ejemplo, la caza intensiva ha podido contribuir a la extinción local de
la amenazada perdiz pardilla Perdix perdix (Watson et al. 2007). Aunque esta última
especie es considerada de interés cinegético, sus poblaciones han sufrido un gran
declive hasta el punto que su caza tradicional a dejado de ser sostenible (Aebischer
1997). Durante nuestro período de estudio, este grave problema de sobreexplotación
sólo fue observado en el coto donde la suelta de perdices era la base de la gestión.
A pesar de que la sobreexplotación cinegética podría estar especialmente ligada
a ésta práctica de gestión, esto no ocurre siempre. Siendo en aquellos casos en los que la
caza se mantiene como un aprovechamiento de temporada y únicamente gestionan la
perdiz en el período de suelta (control de depredadores, agua y alimento suplementario),
en los que tienden a producirse con mayor probabilidad sobreexplotaciones. En tales
enclaves la presencia de la perdiz esta íntimamente vinculada a las sueltas con aves
procedentes de granjas, y de poco o nada sirve una gestión adecuada del hábitat. Por
otro lado, nos encontramos otros casos que mantienen la gestión durante todo el año, en
los que la gestión cinegética juega el papel principal y donde una adecuada gestión del
hábitat puede ayudar a mantener (incluso en cotos de caza intensiva con sueltas de gran
cantidad de perdices) un stock reproductivo base.
Otro de los riesgos potenciales de las sueltas, como es la transmisión intra- e
inter-especifica de parásitos intestinales, también puede suponer una amenaza para la
conservación de la biodiversidad (Tompkins et al. 2001; Villanúa et al. 2007), y de las
propias poblaciones silvestres de perdiz (Villanúa et al. en prensa). En nuestra área de
estudio, se ha constatado igualmente tanto el riesgo de transmisión interespecífico
170
Síntesis
(Villanúa et al. 2007), como intraespecífico de parásitos intestinales (Villanúa et al. en

prensa). Por otro lado, y tal y como adelantábamos en la Introducción, la ausencia de
información en lo que a parásitos sanguíneos se refiere, dejaba vacío un campo de
investigación que precisaba de un análisis detallado, ya que la diseminación de las
enfermedades causadas por estos protozoos (géneros Plasmodium, Haemoproteus o
Leucocytozoon) puede tener importantes consecuencias en la dinámica poblacional de
las aves (Valkiūnas 1993; Merino et al. 2000). Los resultados obtenidos en el capítulo 4
de esta tesis doctoral añaden los parásitos sanguíneos al ya amplio grupo de posibles
amenazas de las sueltas de perdices procedentes de granja. En primer lugar,
encontramos unas prevalencias de parásitos sanguíneos muy altas para aves de estos
ambientes, y muy superiores a las encontradas recientemente en un ave que comparte
hábitat con las perdices, en una zona de estudio cercana y usando una metodología
similar (Ortego et al. 2007). Puesto que, paralelamente, hemos detectado que la malaria
puede invadir de forma explosiva las poblaciones de perdices de granja (García et al.
datos no publicados), es posible que las prevalencias anormalmente altas de las perdices
sean otro efecto negativo no deseado de las sueltas de aves de granja. Encontramos,
además, una asombrosa variabilidad genética a pequeña escala geográfica en los linajes
de parásitos sanguíneos que se explica principalmente por las diferencias entre cotos
donde existe presencia de perdices procedentes de suelta o no, lo que vendría a sugerir
que la suelta de perdices puede estar introduciendo linajes de parásitos sanguíneos
nuevos en las poblaciones silvestres.
A pesar del cada vez más amplio conocimiento sobre las diferencias entre las
comunidades de parásitos de aves de granja y silvestres (Millán 2004; Villanúa 2007),
poco se sabe acerca del papel de estos parásitos sobre la eficacia biológica de las
perdices (Blanco-Aguiar 2007). Dados los hallazgos comentados anteriormente, urge
una investigación detallada sobre los efectos de los parásitos sobre variables como la
condición física, la inversión en cuidados parentales, el éxito reproductor, o la
supervivencia. Para ello el desarrollo de estudios experimentales sería de gran ayuda.
Finalmente, el riesgo de alteración genética de las poblaciones silvestres de
perdiz es un hecho constatado y ampliamente distribuido por la península Ibérica
(Blanco-Aguiar 2007), especialmente en áreas donde se han soltados perdices con fines
cinegéticos (Blanco-Aguiar 2007). A pesar de la reducida eficacia de las sueltas
(Gortázar et al. 2000; Perez et al. 2004), es conocido que las perdices de granja pueden
llegar a sobrevivir y criar en el campo (Duarte & Vargas 2004). Nuestros resultados son
171
los primeros que aportan datos sobre la reproducción de estas perdices híbridas en el
medio natural. Un resultado importante es la más baja supervivencia detectada en
individuos híbridos, incluso una vez superado el período crítico de las primeras semanas
después de la suelta, en el que es bien conocida la alta mortalidad que sufren (Gortázar
1998). Una de las causas de esta menor supervivencia podría ser una mayor
susceptibilidad a la depredación a largo plazo y no sólo las semanas después de la
suelta, como parecen indicar nuestros resultados. Otra explicación alternativa sería la
asociación entre algunos parásitos y variables fisiológicas, que podrían ser un indicativo
de posible pérdida de adaptación local de las perdices híbridas frente a los parásitos
locales (Blanco-Aguiar 2007). En cualquier caso, este resultado sugiere que, a largo
plazo, los híbridos tenderían a desaparecer de las poblaciones. Sin embargo, también
encontramos que las perdices híbridas tienen mayores tamaños de puesta, y los machos
híbridos, mayor tendencia a incubar. Estos resultados indican, por tanto, que el éxito
reproductivo de las perdices híbridas en libertad podría ser mayor. Se necesitaría más
información sobre aspectos no abarcados hasta el momento, como el éxito de
emparejamiento o la supervivencia de pollos de perdices híbridas, para desarrollar
modelos demográficos que permitan aclarar si los genotipos híbridos tenderían a
extenderse o a desaparecer en poblaciones que no estén sometidas a nuevos refuerzos
con híbridos. Esta información sería importante para desarrollar una estrategia de
gestión efectiva para conservar la pureza genética de la perdiz roja silvestre.
En general, el origen de la amenaza que ahora nos encontramos en el campo, en
parte no está en las propias sueltas si no en el estado sanitario y genético de las aves
procedentes de las granjas. Cuando se comenzó a usar este sistema de gestión no parecía
haber demasiada preocupación sobre lo que se estaba soltando al campo, y en un año tan
reciente como 1992, se hablaba con libertad sobre la existencia en las granjas de
perdices que procedían de cruces sucesivos entre A. rufa x A. chukar o A. rufa x A.
graeca (Nadal 1992). En cuanto al estado sanitario, en un estudio realizado
recientemente en las granjas de perdices de la provincia de Ciudad Real, se ha
comprobado que la gestión sanitaria es prácticamente inexistente cuando no
completamente desconocida (Martínez-Lorca 2002). Sólo muy recientemente ha
comenzado a surgir una cierta preocupación sobre la calidad genética y sanitaria de las
perdices de suelta, siendo urgente aplicar los métodos de detección de híbridos y de
gestión sanitaria para mejorar la calidad de los ejemplares que están siendo liberados.
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Síntesis
Las administraciones han comenzado también a tomar cartas en el asunto, aunque de

forma mucho más tímida y lenta de lo deseable.
Podría pensarse que la solución a este problema, y así se reclama desde los
sectores más extremistas, sería prohibir esta técnica de gestión. Sin embargo, nuestros
resultados indican que en el campo las perdices híbridas podrían ser incluso más
productivas que las rojas, y por tanto, a la espera de información más detallada que
permita desarrollar modelos demográficos, no consideraríamos aconsejable eliminar
completamente las sueltas, ya que los genotipos híbridos podrían estar extendiéndose en
las poblaciones incluso sin recibir refuerzos adicionales de perdices de suelta. Por el
contrario, y apoyándonos en la nueva Ley de Patrimonio Natural y Biodiversidad, que
dice que las administraciones públicas competentes velarán por que las sueltas y
repoblaciones con especies cinegéticas no supongan una amenaza para la conservación
de estas u otras especies en términos genéticos o poblacionales, la solución podría estar
en la misma técnica que creó el problema: sueltas con perdices de buena calidad
genética, asociadas a caza intensiva, estrategia que contribuiría a revertir la estructura
genética de las poblaciones.
Importancia de las reservas de caza
Tan importante como evaluar las estrategias de gestión cinegética es valorar el

efecto indirecto del desarrollo de la caza. Durante la práctica de esta actividad de alto
impacto, son muchas las especies que pueden verse directa o indirectamente implicadas.
Existen numerosos estudios realizados principalmente en ambientes acuáticos, pero
también en otros hábitats, que aportan resultados reveladores sobre el efecto de la caza
en el comportamiento y distribución de distintas especies (Madsen & Fox 1995; Fox &
Madsen 1997; Duriez et al. 2005; Klaassen et al. 2006; Thiel et al. 2007; Thiollay
2007). Sin embargo, hasta donde sabemos, no existe ningún trabajo realizado en áreas
agrícolas sobre el efecto de la caza en el comportamiento de las aves, a pesar de que en
estos hábitats la caza es un aprovechamiento alternativo al uso de la tierra muy
extendido (Bernabeu 2000; Howard & Carroll 2001; Martínez et al. 2002). El trabajo
presentado en el capítulo 5 de esta tesis doctoral, se desarrolló en Francia, donde está
muy extendido el uso de reservas de caza dentro de los cotos. En estas reservas distintas
especies podrían encontrar refugio porque no está permitido cazar.
173
Nuestros resultados mostraron que en las tres especies estudiadas (sisones,

avefrías y chorlitos dorados) la actividad cinegética inducía cambios de comportamiento
que podrían suponer mayores gastos energéticos. También comprobamos que las
reservas de caza cumplían una función importante, actuando como refugio eficaz en los
días que se desarrollaba dicha actividad. Además, los resultados sugieren que la caza
puede ser un estímulo adicional que desencadene la migración en los sisones. Aunque
este trabajo se realizó en el centro oeste de Francia, estos resultados podrían ser
igualmente extrapolables a zonas agrícolas del centro peninsular, donde están presentes
las tres especies estudiadas junto a otras como la ganga ibérica (Pterocles alchata), la
ganga ortega (Pterocles orientalis) y la avutarda (Otis tarda). Aunque en España existe
la figura de las reservas de caza dentro de cada acotado. La normativa vigente a nivel
estatal, o en cada caso concreto para cada comunidad (aquellas que hayan desarrollado
una ley de caza) es la que regula a través de los planes técnicos de caza la distribución y
tamaño de tales enclaves. En concreto para Castilla-La Mancha, sólo aquellos terrenos
cuya superficie sea igual o superior a 500 hectáreas, deberán reservar del ejercicio de la
caza al menos un 10 % de la superficie total del coto. Si bien aunque se cumple la
normativa, estas zonas suelen situarse en áreas de menor valor faunístico. A pesar de
ello, sería importante desarrollar este tipo de trabajos en zonas del centro peninsular,
añadiendo otras especies de gran interés de conservación e incluyendo a las especies
objeto de caza. A su vez, comprobar la utilidad de las reservas de caza fuera del período
hábil (éxito de reproducción y mortalidad dentro y fuera de las reservas), sería un
importante paso previo a la creación de una red de refugios para establecer una pautas
generales de gestión, que puedan beneficiar tanto a especies cinegéticas como a otras
presentes en los mismos hábitats.
EPÍLOGO: Integración de conservación, gestión agrícola y gestión cinegética
Para integrar conjuntamente el aprovechamiento cinegético y agrícola, junto a la

conservación de la biodiversidad, se precisa tener una percepción lo más completa
posible de los efectos y consecuencias de los distintos modelos de gestión agrícola y
cinegética en la conservación de las especies de aves que comparten un mismo medio.
En nuestro caso, hemos basado la estrategia en estudiar los principales factores que
pueden afectar a la viabilidad poblacional de la perdiz roja. Teniendo en cuenta la
importancia socioeconómica y las particularidades ecológicas de esta especie, la perdiz
174
Síntesis
roja puede llegar a desempeñar la función de especie “paraguas” (al igual que sucede
con muchas otras especies cinegéticas) dentro del ecosistema, y en consecuencia, que
muchas de las acciones encaminadas a mejorar el rendimiento y conservación de sus
poblaciones, puedan resultar beneficiosas o no para otras especies que comparten su
territorio.
Por lo que respecta a la gestión del hábitat (agrícola), según los resultados
presentados en esta tesis doctoral, podemos establecer una serie de medidas que podrían
adoptarse en beneficio mutuo, tanto de las poblaciones de perdiz roja, como de las
poblaciones de aves esteparias amenazadas, principalmente:
- Incremento y/o mantenimiento de las lindes y fomento de medios de cría

alternativos al cereal, en particular barbechos. En particular, para conseguir
estos objetivos se debería mejorar la aplicación de la normativa de eco-
condicionalidad de la PAC.
- Retraso de las fecha de cosecha, al menos en las bandas externas de las
parcelas de cultivo.
- Mantenimiento del mosaico paisajístico característico de las áreas agrícolas.
En el caso de los problemas derivados de las sueltas, como son la introgresión

genética, y la transmisión de parásitos, quizás el principal riesgo no estribe en la suelta
de perdices per se, sino en el origen genético y control sanitario de las aves en las
granjas previamente a la suelta. Hasta el momento los protocolos de control sanitario
adoptados, no son lo suficientemente eficientes como para evitar la introducción de
nuevos parásitos en el campo (Villanúa et al. 2007b). Por ello, mejorar y aplicar nuevos
protocolos de control sanitario y genético debe ser una de las prioridades en la que las
distintas administraciones deben centrar sus objetivos. Según los resultados presentados
en esta tesis doctoral podemos establecer una serie de medidas que deberían adoptarse
para mejorar la calidad de las perdices soltadas y para preservar las poblaciones
silvestres “puras”:
- Aplicación real de la legislación que prohíbe la suelta de perdices no

autóctonas, mediante controles genéticos de las granjas de producción.
- Mejora en la normativa sanitaria y exigencia de aplicación de programas de
gestión sanitaria.
175
- Detección de áreas críticas para la conservación de la pureza genética de la

perdiz roja silvestre, en las que se debe impedir la llegada de híbridos
procedentes de sueltas.
- Marcaje estable (anilla metálica) de todas las aves liberadas de granja, para
su posterior control y seguimiento.
Por último, el establecimiento de una red de reservas enclavadas en zonas de

gran riqueza faunística, en lugar de situarla en zonas marginales que realmente no tienen
ningún efecto sobre las poblaciones de aves, podría ser una medida mucho más efectiva
que la actual distribución de áreas de reserva.
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CONCLUSIONES
Conclusiones
1- La perdiz roja es una especie cinegética con alta productividad, la variabilidad

encontrada entre años en tamaños de puesta, tasa de incubación de machos,
fechas de inicio de puesta y éxito de eclosión, apuntan al clima como factor de
especial importancia sobre estos parámetros. Esta condición debe tenerse en
cuenta a la hora de diseñar los planes estratégicos de gestión.
2- Los machos de perdiz roja juegan un importante papel en el éxito reproductivo.

Alrededor del 50 % de los machos pueden hacerse cargo de la incubación de un
nido, salvo en años donde la productividad general de la especie es muy bajo.
Por tanto, aunque el hecho de que los machos incuben pudiera parecer un
comportamiento anecdótico carente de importancia, en realidad su contribución
a la productividad de una población de perdices es importante.
3- Cambios en la gestión agrícola serían más efectivos para mejorar el éxito

reproductivo de la perdiz que el control de depredadores en zonas agrícolas.
Particularmente el mantenimiento y creación de lindes, así como un retraso en la
fecha de cosecha, al menos en la franja más externa de las parcelas de cereal.
Estas disposiciones deberían ser consideradas una prioridad entre las medidas de
eco-condicionalidad de la PAC.
4- El impacto negativo de la cosecha en el éxito reproductivo de la perdiz roja ha

sido detectado en otras especies de importancia conservacionista, esto podría dar
lugar a generar programas de colaboración entre agricultores, cazadores y
conservacionistas que beneficiarían a un gran número de especies.
5- La suelta de perdices procedentes de granja supone una amenaza para la

integridad genética de la perdiz roja. La situación podría empeorarse por los
mayores tamaños de puesta de las hembras híbridas. Controlar la introgresión de
genomas alóctonos es una pieza de vital importancia para la conservación a
largo plazo de esta especie. Proponer urgentes programas de gestión que
detengan la suelta de perdices híbridas, renovar los pools genéticos en áreas con
introgresión genética, y preservar las poblaciones en buenas condiciones
genéticas son medidas imprescindibles para la conservación de esta especie.
6- La suelta de perdices procedentes de granja es un importante factor que afecta a

la distribución de los linajes de parásitos sanguíneos a escala local. Valorar las
consecuencias del manejo humano sobre los hospedadores, en este caso la perdiz
roja, es esencial para comprender las implicaciones de tales acciones para la
conservación de la vida silvestre y el control de enfermedades.
7- Las reservas de caza juegan un papel crucial para la gestión de las especies
cinegéticas y para la conservación de especies amenazadas en áreas agrícolas.
Incrementar el tamaño o el número de reservas podría ser una importante
herramienta de gestión y conservación para reducir el impacto de la actividad
cinegética. Retrasar la fecha de inicio de la caza en áreas donde existen
poblaciones de sisón común migratorias, sería una importante medida para
reducir el efecto de la caza sobre esta especie. El plan de gestión debería
también estar integrado por la creación de una red de refugios a escala
internacional.
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8- La caza es una actividad que causa perturbación en el comportamiento y

distribución de muchas aves que ocupan el mismo hábitat donde se realiza tal
actividad, lo que puede tener importantes implicaciones a nivel de comunidad.
La perturbación asociada a la caza induce cambios de comportamiento que
podrían suponer mayores gastos energéticos.
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AGRADECIMIENTOS
Agradecimientos
Si no recuerdo mal, fue antes de mi etapa de párvulos cuando comencé a tener

claro a que quería dedicarme de mayor, sería más o menos a la misma vez que aprendí a
atarme el cordón de mis zapatillas. Después de esa época, quizás las ideas de un niño
pueden cambiar mucho. Ya se sabe, la adolescencia, el aumento de los niveles de
testosterona, el descubrimiento de nuevos mundos, el lado oscuro de la luna, pero ése,
afortunadamente no fue mi caso. Puede que Félix Rodríguez de la Fuente tuviese mucho
que ver. Esta frase es muy repetida por muchos de los que amamos esta profesión, pero
es que sin duda, para los de mi generación y otras precedentes Félix nos mostró la
naturaleza de una manera tan atractiva que era muy difícil no sentirse cautivado. Aún
hoy día, sigue siendo referente para muchos naturalistas, tanto aficionados como
profesionales. Valga desde aquí mi agradecimiento a la persona que lanzó a correr el
sentimiento latente de mi vocación. Y digo latente, porque no me imagino haciendo otra
cosa.
Si hay alguien que por encima de todo el mundo merezca mi agradecimiento,

son sin duda mis padres y mi hermana Gema, que siempre han tenido plena confianza
en mí y me han apoyado en todo lo que me he propuesto. Gracias, no solo por respetar
mi decisión de dedicarme a lo que realmente me gusta, estudiar a los pájaros, sino
también por participar y disfrutar de ello conmigo. Que un día de lluvia te llegue tu hijo
a casa lleno de barro, en cero con dos te monte en la cochera un laboratorio móvil,
saque una perdiz de una bolsa, y te diga que la sujetes que tiene que sacarle sangre,
después se vaya corriendo y te dejé la cochera llena de barro y plumas, no basta solo
con quererlo para no mandarle más allá de Fernando Po. Juntos habéis conseguido que
me olvide del resto de menesteres y quehaceres, para que me ocupase única y
exclusivamente de la tesis (cuantas veces habré escuchado que vivo en un “hotel”), y de
mis continuas juergas y viajes (mi segunda ocupación). Es por ello que esta tesis no solo
va dedicada a ellos, sino que a pasado a formar parte de ellos. ¿A ver a qué nos
dedicamos ahora? Tendré que echarme una novia. En fin, gracias por vuestro cariño,
pero sobre todo por ser los mejores padres y hermana del mundo.
Por otro lado, afortunadamente cuento con una familia a la que adoro, y que han
estado siempre apoyándome. Cuantas comidas y cenas rodeado de ellos, siempre
presentes, tanto en lo bueno como en lo malo. Este “bichologo” como me dicen mis titas
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“las Bartolas” (Estrella, Jose, Monchi y Santi), tiene mucho que agradecerles por estar
siempre ahí, porque sentir el apoyo de la familia unida te empuja a lograr tus sueños.
Nada me hubiese gustado más que mi abuelo Santiago pudiera disfrutar conmigo
de este momento, gracias por las innumerables charlas sobre pájaros, por dejarme
compartir contigo mi pasión, pero sobre todo por tu cariño. Allá donde estés te llevo
conmigo junto a mi primo Alberto, a quién también va dedicada esta tesis. Albertillo, mi
fiel escudero, fuiste David contra Goliat en una batalla que no pudiste ganar, pero tú
coraje y tú fuerza siguen vivos en mi.
Mis primos Carlos, Chulé, Fran y Javi en algún momento han sido parte activa
de esta tesis cuando precise de un ayudante de campo. Sobre todo tengo que
agradecérselo a Carlos “el limón”, que nunca puso pegas, cuando le sacaba de la cama
temprano los fines de semana. Y si no era para eso, era porque le tocaba ir con Fran o
mi padre a entrenar al equipo de fútbol benjamín, que estuve entrenando el primer año
de tesis, y al que los períodos de capturas no me dejaban atender. Ya se, que con unas
palabras de agradecimiento no bastara, y me tocara pagar unas copas, pero todo a su
tiempo.
Si me pongo a dar las gracias a mi familia me podría extender eternamente,
porque son muchos momentos vividos junto a ellos, tanto durante el desarrollo de esta
tesis como durante el resto de mi vida, que tendré que cortar por algún lado. Gracias a
todos por vuestro cariño y apoyo. Al resto de mis abuelos, especialmente a mi abuela
Josefa, a mis titos Carlos, Fran, Jesús, José, Mento y Tomás, al resto de mis primos, a
mis primas-titas las “mayorettes” (Cefe, Mari y Santi), a mi tío Agustín, mis tías Pacica
y Crece, y a Justito. Disculpad si me dejo alguno, espero que no os sintáis ofendidos, la
lista es larga y cada uno sabe perfectamente el cariño que le tengo y el granito de arena
que han aportado al desarrollo de este trabajo.
Mis directores se han ganado el cielo conmigo, Javi y Francois, os tengo mucho
que agradecer, y no solo a nivel académico, gracias por vuestra amistad y confianza.
Además, yo sé que el sentimiento es mutuo, si no, no se vestirían de toreros en la fiesta
de celebración de mi tesis. Francois se que ha estado ensayando “el paseíllo”. De lo que
son capaces mis directores porque su doctorando se sienta a gusto, ¡que arte!.
Javier Viñuela “Viñu” ha estado presente desde el inicio de la elaboración de
esta tesis, ha sido mi maestro y mentor en esto de la ciencia, y la persona que más veces
me ha llamado “golfo” del mundo mundial. Javi, muchas gracias por confiar en este
188
Agradecimientos
churriego, a pesar de lo que dice el Quijote de las gentes de mi pueblo, y que tantas
veces me has repetido. En el fondo llevas a Miguelturra en tu corazón, y ahora más
todavía que tu hija es churriega. Bromas a parte, mucho ha sido lo que me has aportado,
y mucho lo que he aprendido de ti, tu elegante mano izquierda, tu cercanía, ese afán de
superación, a seguir trabajando incluso cuando uno esta de juerga… No me imagino
haciendo la tesis con otro director que no seas tú, has sabido darme el punto justo en el
momento que lo necesitaba, y sobre todo me has dado libertad absoluta para tomar mis
propias decisiones. Incluso en otros tiempos cuando existían otro tipo de
preocupaciones, siempre conté con tu apoyo. Gracias por todo jefe, compañero, amigo.
Francois Mougeot llego en la última fase, pero justo en el momento para
rescatarme y darme una “patada en el culo” para espabilarme. Gracias por no dudar en
ningún momento en apoyarme cuando lo solicite y sobre todo por guiarme por el
estrecho y tortuoso laberinto de la estadística (ya no me da miedo). Para mi ha sido un
autentico privilegio tenerte como director y gozar de tu amistad. Esa capacidad que
tienes para hacer fácil lo difícil, sin lugar a dudas me ha abierto mucho los ojos, y me ha
sacado del atascamiento mental en más de una ocasión. Dicen que detrás de un gran
hombre siempre hay una gran mujer. Para mi sois igual de grandes los dos, y por eso
también quiero incluir en este apartado a tu mujer, Bea Arroyo, que entre las sombras ha
estado apoyándome cuando lo necesite. Gracias a los dos, porque vuestra llegada
supuso el empujón final para esta tesis que por fin ve la luz. Por último, gracias por
regalarme parte de tu arte como queda plasmado en el dibujo de la portada de esta tesis.
Txuso García, más conocido por mi familia como el pedigüeño, ha sido otra
pieza clave para la elaboración de esta tesis. Gracias porque tus sugerencias y apoyo han
sido fundamentales para que de una vez por todas termine. María jugó también un
importante papel, aportando su trabajo de laboratorio. Txuso, aún no te puedo agradecer
que me invites a las barbacoas de tu casa, porque todavía no la has estrenao, pero ya
sabes lo que te toca Neng. Ahora que tendré más tiempo tenemos que crear el
diccionario Francois-Español Español-Francois, que para el primer tomo ya tenemos
material.
Esta tesis ha sido desarrollada sobre un tema que no solo atañe a aspectos
biológicos, sino que también se han visto inmersos aspectos sociológicos, dado el
importante calado que tienen en nuestra sociedad tanto la caza como la agricultura. Por
189
eso desde un principio he tenido que contar con la colaboración de un gran número de
personas. Todo el trabajo que se ha desarrollado no hubiera sido posible sin el apoyo de
los cazadores de Miguelturra. Mención especial merecen, la junta directiva de la A. D.
La Tonela, así como Lorenzo Sobrino, Jose Juan Bermejo, Mariano Rodrigo, Pedro
Martínez, Ángel, Raúl y Delfín Martín de Lucía, por facilitarme la labor y su amable
disponibilidad siempre que he requerido de su colaboración. De entre todos los que han
colaborado durante el desarrollo de este trabajo, Inocencio Bastante (presidente de la A.
D. La Tonela) ha sido sin lugar a dudas el que más me ha facilitado el trabajo. Gracias a
tu implicación y tu apoyo esta tesis es hoy una realidad, personas como tu son las que le
dan sentido al desarrollo de este tipo de trabajos.
Durante los años de duro trabajo de campo me encontré con un inesperado
compañero, sin cuya aportación esta tesis hubiera perdido buena parte del enfoque
social que precisaba. Ambrosio, muchas gracias por tu apoyo y por no dudar en ningún
momento en prestarme tu ayuda, pero sobre todo por transmitirme tu cariño. No
recuerdo ninguna conversación contigo en la que no hayamos acabado riéndonos.
Gracias a tu compañía el trabajo de campo se hizo mucho más llevadero.
En general, gracias a todos mis amigos por mantenerme los pies en el suelo y
sacarme (al menos temporalmente) los pájaros de la cabeza. Pero sobre todo, porque
aunque mis continuas ausencias me impiden disfrutar de vosotros más de lo que me
gustaría, vosotros rompéis esa distancia física, haciéndome sentir como si estuviésemos
juntos todos los días (aunque sea de juerga en juerga, y gracias a que no me pierdo una).
Gracias, para mi tiene mucho valor sentir vuestro apoyo y cariño. Sois muchos y me
siento afortunado por ello, pero dejar de casaros que me vais a arruinar.
“Que ricos los chorizos parrilleros, los chorizos parrilleros…” Gracias chicas
Ana, Cristina, Elena, Esther, Irene, Guadalupe, Pili y Uge, y chicos Chiky, Chory,
Congui, Cristian, Javi, Juan Angel, Manolo, Oscar, Sabanilla, Víctor, Villu, Yenca y
Yiyo, simplemente por estar ahí.
A los con esa cara Jarcho, Nico, Diosco, Alfonso, Martinillo, Rifle y Peri.
Julio gracias por sacarme de mi mundo y abrirme los ojos, tenemos que
recuperar el tiempo perdido. A Panico, Guiller, Yepes, Julito “motos”, David “el
herrero” y compañía por esos carnavales inolvidables, “Que arda Troyaaaaaaaaaaa…”.
A Antonio “Canani” que fue mi compañero de batallas hasta que se puso a hacer niños.
A Federico Valero por su apoyo y perseverancia.
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Agradecimientos
Con mis amigos de la facultad he vivido una de las etapas más importantes de mi
vida. Graná no hubiera sido lo mismo sin vosotros, sin las fiestas en el Bar-Tolo, las
cañitas después de clase, las Cruces, la fiesta de la primavera, Chite, los viajes a la
playa, la reunión de navidad, la excursión a Montilla, el arroz Strogonoz, los
bioencuentros (porque nunca sabes lo bueno que puedes llegar a encontrar), etc., en fin,
mil y una vivencias. Gracias a las niñas Bea, Cecilia, Eva, Juani, Guada, Laura, María
Luisa, María P., María T., Marta, Mercedes, Raquel, Sonia y Yoya, y a los chavales
Alvaro, Carlos, Dj Lacal, Javi, Jesús Caro, Jesús “Prodigy”, Luiso, Platero y Rober.
Con Jesús “Prodigy” y Jesús Caro, además de todo lo anterior me une compartir
gustos y aficiones, y con ellos realicé mis primeros acercamientos al mundo de los
pájaros en el medio natural. Que buenos momentos pasamos en nuestras primeras
jornadas de campo por el Sotillo de Iznalloz, que cara de tontos se nos puso cuando
escuchamos a nuestro primer búho real, no se me olvidara nunca esa noche. Jesús
“Prodigy” es un gran artista, como demuestra en el dibujo que abre esta sección, ten
amigos para esto, “ende luego”. De corazón gracias, por esos magníficos dibujos que
has realizado para mi tesis.
A Irene y Vero (“primaaaaa”) porque sois dos soles y valéis un montón, que no
se os olvide nunca.
Los miembros de SEO Ciudad Real (Carlos, Jose Luis, Jose Manuel, Carmen,
Prado, Rafa, Benito, Alejandro…) son como una pequeña familia, que es lo que
realmente le da valor a este tipo de asociaciones, gracias a todos. Sobre todo a Juanito y
Angel con quienes he compartido muchos momentos de alegría, pero también de
agobio, menudo trabajito nos costo sacar adelante el anuario. De Luis Segura no tengo
más que buenas palabras, has sido sigiloso pero se que estabas ahí, muchas gracias por
tu apoyo. Además, sin tus bolis, libretas y demás accesorios no sé como hubiera tomado
los datos en el campo, gracias amigo. Igualmente gracias Javi por tu apoyo, por fin
podré ponerme con tus datos.
No puedo olvidarme de las “zapatilleras”, porque 5 años dan para mucho, y hay
momentos para todo. El campo, las flores, la primavera, la testo, es lo que tiene …
Ahora toca agradecérselo a la peña del IREC, puff casi na, después de más de 5
años aquí, el IREC es como mi segunda casa (aunque algunas veces creo que ha sido la
primera, sólo me ha faltado quedarme a dormir). Comenzaré por mis compis de
191
despacho, que son los que más me han sufrido, sobre todo por mí afición a gastarles
bromas y a la buena música. Nuestro despacho en más de una ocasión parecía más bien
el camarote de los hermanos Marx, sobre todo porque he cambiado más de compañeros
que la Obregón de novio. Empecé con Paquillo, Jota, Salva y Linares, aunque en esa
primera etapa apenas pisaba el despacho (demasiado campo). Jota gracias por tu apoyo
en los momentos que necesite de tu experiencia. Paquillo eres un artista y ahora que eres
churriego no te digo na. Con Linares compartí muchos buenos momentos en el campo,
hasta que nos acusaron de cazar perdices con arco (la antena del radio-seguimiento
menudas flechas lanza!). Los ruidos de tu estomago, las bolsas de cheetos para
desayunar, y nuestras eternas charlas sobre caza y conservación me han hecho pasar
muy buenos momentos. En Salvatore encontré un gran amigo y compañero no solo de
curro si no también de juergas, menudas hemos montao por el torreón (y las que nos
quedan). Gracias por ser de los pocos que han aguantado el ritmo de curro-juerga, sin ti
el trabajo de campo hubiese sido muchísimo más duro.
Después hubo remodelación en el despacho, Jota y Paquillo se fueron a vivir al
zulo, y yo me quedé con Loren, Gustau y Paco. Con Loren además me unía compartir
director, que ojo tuvo el Viñu para juntar a dos becarios tan distintos (vamos eso dice él,
porque yo no creo que seamos tan diferentes), pero que se entienden tan bien. Sin lugar
a dudas serás uno de los científicos más brillantes que salgan del IREC, para mi es un
autentico privilegio trabajar contigo. Gracias por estar siempre que he necesitado tu
ayuda, por no negarte en ningún momento a mis múltiples y variopintas proposiciones
(todas decentes, eh!), pero sobre todo por tu amistad, eres un crack my friend. Por
supuesto, gracias por prestarme unas pinceladas de tu arte. Gustau “electrobugy master
breaker”, que paciencia has tenido conmigo, y que buenos ratos he compartido contigo
estos años. Ché gracias por tu apoyo y ayuda. Paco “el trampero” raro ha sido el día que
no nos hemos echado unas risas, gracias por esos momentos. Por aquel entonces
también tuvimos de artista invitado a Txuso, aunque duro poco, quiso tener su propio
camerino. A pesar de tanto cambio, no penséis que esto se quedo así, hubo uno más.
Loren y Gustau se fueron, y llegaron Jose Luis “Melendi” y Jesús Caro (las vueltas que
da la vida) para acompañarnos a Paco y a mi. Melendi, compañero, tu si que tienes
paciencia, te ha tocado vivir la fase más estresante de la tesis, y te toco ser el saco de
boxeo donde descargar la adrenalina (no vayáis a pensar que le daba de hostias, que no
hablaba en sentido literal).
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Agradecimientos
Pero el IREC es muy grande, y no solo hay vida en el despacho, fuera también
he encontrado grandes amigos y compañeros. Diego el terror de Huesca, gracias por
esos momentos de perdices, liebres y cubatas, que padrazo que vas a ser. Miguel que
momentos hemos pasado hablando de zapatilleras, jeje. Gracias por consolarme ante el
desesperante retraso de los revisores con los artículos. Carlitos empezamos juntos y
vamos a terminar juntos, hemos compartido muy buenos momentos Hannover,
carnavales, feria de abril, y un largo etcétera de eventos festivos, todos a cual mejor. Si
me quiero ir de fiesta me voy contigo ¿a ver como no lo montamos al final?. Luis
Enrique “Vilches” que “lo mismo vale pa un roto que pa un descosio”. La próxima vez
que vayamos de comida no te lleves la caña para pescar, tu ya sabes Tomaaaas!. Pablo
(barbakiu-man) y Paqui (La Celestina que no pudo conmigo, aunque mira que lo
intento), gracias por estar siempre ahí, y enhorabuena por ese retoño que llega. A Inés
por su sonrisa y su impagable trabajo de laboratorio. A las chaparreras, Elenis y Raspa
por su dedicación y trabajo que debe ser un ejemplo para muchos. A Dávila por sus
momentos de concupiscencia y esos mails que no se de donde los saca, pero que son la
leche. A Silvia por su tesón y su sonrisa, no te rindas nunca. A Nuria y Cat las últimas
adquisiciones de ecología. A Javitxa “el chino” por lo bien que conduce cuando hay
barro. A las chicas de la planta de abajo (submundo) Eli, Vane, Victoria, Mari Paz,
Dolo, Mónica, Isabel, Sandra, Mariana y Raquel; y a los chicos Pelayo, Fran, Joaquín y
Manolo. A Christian Górtazar, Pablo Ferreras, Rafa Villafuerte, Paqui Castro, Ursula
Hofle y Rafa Mateo porque en más de un momento he podido disfrutar de su ayuda. Al
clan ungulata Marisa, María, Nacho y Jorge Cassinello. A Jesús Carrasco por su apoyo
incondicional. Aunque apuntas maneras como “mataor” te falta manejo con el capote,
pero habrá que darte la alternativa. A Carlos Alonso por la gran castaña del primer día
que salimos de juerga juntos y porque se disfrazara de cazador en la próxima fiesta
(aunque sea de los años 60). A todos los alumnos de prácticas que pasaron por el IREC
durante la realización de este estudio, especialmente a Laura y Yoli.
Al personal de administración por su ayuda y paciencia con todos los trámites
necesarios, especialmente a Arturo (el Genovés).
A las mujeres de la limpieza, especialmente a Angelines porque recordarme en
más de una ocasión que el IREC no era mi casa, y sobre todo por contener sus impulsos
para no acabar con la entropía y el caos que habita normalmente en mi mesa.
A Jorge, Vicente, Terry y Javi los vigilantes por esos ratos de charla en la garita.
193
A Julián Garde que tiene una paciencia fuera de lo normal, por ayudarme y
resolver todas mis dudas con los papeleos de la tesis.
De fuera del IREC, a Vincent Bretagnolle por su apoyo y ayuda durante mi

estancia en Chizé (Francia). Igualmente a todos los estudiantes e investigadores de ese
centro por hacerme más agradable mi estancia, especialmente a Carole Attié, Loïc
Hardouin, Alex Millon y Diane Desmonts.
A Carlos Palacín y Pedro Olea por acceder a revisar la tesis a la velocidad del
rayo. Muchas gracias por no dudar en prestarme vuestra ayuda en ningún momento.
A Steve Redpath por su apoyo y confianza. Contigo voy a empezar una nueva
etapa que seguro será tan buena o mejor que ésta. A Jesús Martínez por su ayuda en los
primeros momentos de esta tesis, y por su apoyo para la siguiente etapa por las tierras
de Sir William Wallace.
Y hasta aquí puedo leer, porque como siga con los agradecimientos voy a
terminar dándole las gracias hasta al de la gasolinera. Siento si me he dejado a alguien
sin nombrar que lo merezca, efectivamente lo merecerá, pero disculpad por mi despiste.
Yo quiero una novia que me haga feliz,

si llego borracho que se eche a reír,
si yo no trabajo ni gano un jornal,
a mí que me dejen cantar y bailar.
(Anónimo)
194

Tesis Fabian Casas

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Gestión agraria y cinegética: efectos sobre la perdiz roja

(Alectoris rufa) y aves esteparias protegidas

Memoria presentada por

VºBº los Directores

Dr. Javier Viñuela Madera Dr. Francois Robert Mougeot

INSTITUTO DE INVESTIGACIÓN EN RECURSOS CINEGÉTICOS

Si lo que vas a decir no es más bello

SÍNTESIS ………………………………………………………………………….. 163

Esta tesis esta organizada manteniendo la estructura de cualquier texto científico.

La pseudoestepa agraria (áreas abiertas muy deforestadas principalmente

2. La Perdiz roja: Importancia en el ecosistema mediterráneo

La perdiz roja (Alectoris rufa) es una galliforme de pequeño-mediano tamaño

3. Importancia socioeconómica de la caza de la perdiz roja

En general, la caza es una importante actividad económica que genera

Concretamente, la caza de la perdiz roja es una de las actividades económicas

4. Situación de las poblaciones de perdiz roja

5. Medidas de gestión cinegética aplicadas a la mejora de las poblaciones de perdiz

Dada la recalcada importancia económica, social, ecológica y conservacionista

5.1. Control de depredadores

El control de depredadores es una de las herramientas de gestión más extendidas

tramitación de los permisos de dichos controles (Nadal 1998), ha supuesto a menudo

5.2. Bebederos y comederos artificiales

Otro de los elementos de gestión más extendidos es la colocación de comederos

5.3. Gestión del hábitat

Comunitaria (PAC), a través de las nuevas medidas de eco-condicionalidad, recoja e

5.4. Sueltas de perdices de granja

En esta Introducción, ya se ha hecho referencia repetidas veces a la suelta de

se liberan enormes cantidades de ejemplares en superficies reducidas, y a menudo con

mundial (Aebischer & Potts 1994). La maximización del rendimiento reproductivo

6. Gestión agraria y cinegética como herramientas de conservación en la

La conservación de la diversidad biológica se ha ido convirtiendo poco a poco

aprovechamiento de ambas, sin afectar a la conservación de la diversidad biológica.

conservación comprometido. Las reservas libres de caza podrían actuar en beneficio de

A lo largo de la introducción se ha mencionado en repetidas ocasiones la

variabilidad climatológica interanual, ante la cual pueden adoptar distintas estrategias

interés de las relaciones parásito-hospedador y sus efectos sobre las poblaciones

ADENA. (2006) El veneno en España (1990-2005). Análisis del problema, incidencia y

APROCA. (1998) Valoración económica de la caza en la provincia de Ciudad Real. En:

Arroyo, B. & Beja, P. (2002) Impact of hunting management practices on biodiversity.

Ayala, R. (1985) Adecuación y desarrollo de la oferta de caza menor a la demanda

Baratti, M., Ammannati, M., Magnelli, C. & Dessi-Fulgheri, F. (2004) Introgression of

Bernabeu, R.L. (2000) Evaluación económica de la caza en Castilla-La Mancha. Tesis

Blanco-Aguiar, J.A. (2007) Variación espacial en la biología de la perdiz roja

Cabezas-Diaz, S. & Virgos, E. (2007) Adaptive and non-adaptive explanations for

Calderón, J. (1983) La perdiz roja, Alectoris rufa (L.). Aspectos morfológicos,

De Juana, E. (2005) Steppe birds: a characterisation. En: Ecology and conservation of

Delibes-Mateos, M., Fernandez de Simón, J., Villafuerte, R. & Ferreras, P. (2008)

Díaz, S. (2006) Caracterización de la gestión cinegética y agraria en cotos de caza

Encinas, A. (1982) Plasmodium relictum y P. cathemerium en Aves del área

Gortázar, C., Villafuerte, R. & Martín, M. (2000) Success of traditional restocking of

Lucio, A.J. (1990) Influencia de las condiciones climáticas en la productividad de la

Millán, J. (2004) Alteraciones asociadas a la cría en cautividad de Galliformes

Nadal, J. (1992) Problemática de las poblaciones de perdiz roja, bases ecoetológicas

Pérez-Rodríguez, L. (2007) Señales fiables en la perdiz roja (Alectoris rufa): condición

Rands, M.R.W. (1986) Effect of Hedgerow Characteristics on Partridge Breeding

Rands, M.R.W. (1987a) Hedgerow management for the conservation of partridges

SEO/BirdLife (2006) Seguimiento de las aves comunes reproductoras en España:

SEO/BirdLife (2007) Seguimiento de las aves comunes reproductoras en España:

Tapia, L. & Domínguez, J. (2007). Broad-scale habitat use by red-legged partridge

Tapper, S. (1999) A Question of Balance. The Game Conservancy Trust, Fordingbridge,

Villanúa, D. (2007) Parásitos de la perdiz roja (Alectoris rufa): implicaciones para su

Virgós, E. & Travaini, A. (2005) Relationship between small-game hunting and

Yanes, M. & Suárez F. (1996) Mortalidad en nido y viabilidad poblacional de