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 . In Memoriam .A José Alberto Nieto Arenas. Es mejor caminar que parar y ponerse a temblar …. Revólver) Si lo que vas a decir no es más bello que un silencio. callé el hombre y vuélvase a callar… (Manolo García) . no lo vayas a decir que hablé el mundo y callé el hombre. (Carlos Goñi. . 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 ………………………………………………………………………. 5 2. 18 Bibliografía……………………………………………………………………… 21 CAPÍTULO 1: Doble incubación... 16 Objetivos de la tesis……………………………………………………………..... Gestión del hábitat ……………………………………………….. Medidas de gestión cinegética aplicadas a la mejora de las poblaciones de perdiz ………………………………………….... Situación de las poblaciones de perdiz roja ……. 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 ………………………………………………………………………. 59 Introduction …………………………………………………………………… 59 Material and Methods ………………………………………………………… 62 Results ………………………………………………………………………… 66 i .. 3 1.Índice ÍNDICE ESTRUCTURA DE LA TESIS………………………………………………….. 10 5.. 8 5.2...….. La perdiz roja: Importancia en el ecosistema mediterráneo ……………… 6 3. Sueltas de perdices de granja ……………………………………... 34 Material and Methods ………………………………………………………… 37 Results ………………………………………………………………………… 41 Discussion ……………………………………………………………………........………………………. 45 Acknowledgements …………………………………………………………… 51 References ……………………………………………………………………..… 1 INTRODUCCIÓN………………………………………………………………...4.. Control de depredadores ………………………………………. Importancia socioeconómica de la caza de la perdiz roja………………… 7 4.3.. Gestión agraria y cinegética como herramientas de conservación en la pseudoestepa agrícola ……………………………………………….. Bebederos y comederos artificiales …………………………….. 13 5...... 33 Introduction …………………………………………………………………...1.. 12 5.. 11 5....……. La pseudoestepa agraria ………………………………………. 14 6.........……........ . 137 Material and Methods …………………………………………………….. 99 Acknowledgements ………………………………………………………….. 135 Abstract ……………………………………………………………………… 137 Introduction …………………………………………………………………. en el oeste de Francia: Importancia de los refugios de caza en áreas agrícolas ……... 120 Discussion …………………………………………………………………… 124 Acknowledgements …………………………………………………………. 86 Material and Methods ………………………………………………………... 128 References …………………………………………………………………… 129 CAPÍTULO 5: Efecto de la actividad cinegética en el comportamiento y la distribución espacial del avefría europea....Fabián Casas Arenas Discussion …………………………………………………………………….. 89 Results ………………………………………………………………………... 80 CAPÍTULO 3: Consecuencias fenotípicas y sobre la eficacia biológica de la introgresión genética en poblaciones silvestres de perdiz roja Alectoris rufa …… 83 Abstract ……………………………………………………………………….. 113 Introduction …………………………………………………………………. 157 ii . 74 References ……………………………………………………………………. 85 Introduction …………………………………………………………………. 146 Discussion …………………………………………………………………… 151 Acknowledgements …………………………………………………………... 113 Material and Methods ………………………………………………………..... 116 Results ……………………………………………………………………….. chorlito dorado y sisón común... 70 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? ………………………………………………. 156 References ……………………………………. 111 Abstract …………………………………………………………………….. 93 Discussion ……………………………………………………………………...……………………………. 140 Results ……………………………………………………………………….. 74 Electronic Supplementary Material …………………………………………. 163 Síntesis: Perspectivas de investigación futura y aplicaciones de gestión ... 174 Bibliografía ………………………………………………………………...Índice SÍNTESIS …………………………………………………………………………. 167 Efectos de las sueltas de perdices de granja ……………………………. 176 CONCLUSIONES ……………. 185 i ... 165 Parámetros reproductivos: Nuevos resultados …………………………… 165 ¿Gestión del hábitat o control de depredadores? ………………………. 169 Importancia de las reservas de caza ……………………………………… 173 EPÍLOGO: Integración de conservación y gestión agrícola y cinegética .…………………………………………………… 181 AGRADECIMIENTOS …………………………………………………………….. . de las principales medidas de gestión cinegética y sus efectos. en el apartado de Síntesis se revisan y discuten los resultados obtenidos y sus implicaciones. Aunque las revistas a los que han sido enviados presentas formatos diferentes. pasando por una descripción de la importancia ecología de la perdiz roja en el contexto mediterráneo. como referencias a otros capítulos de la tesis. la caza y la conservación de la fauna silvestre en la pseudoestepa agrícola. Solo se han añadido pequeñas modificaciones. Seguidamente se expone una revisión del estado actual de las poblaciones de perdiz roja. y por último las Conclusiones. se enumeran las principales Conclusiones de la tesis. 1 . Objetivos. Cada uno de los cinco Capítulos sigue la estructura típica de un artículo científico. Por último. y como compatibilizar las actividades tradicionales humanas. Están redactados en inglés. así como de la importancia socioeconómica de su caza. comienza con una descripción del hábitat principal donde se ha desarrollado la toma de datos de esta tesis. 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. que se desarrollaran en cada uno de los cinco capítulos. Finalmente. o explicaciones algo más detalladas de algunos aspectos. un apartado de Síntesis general. así como de enunciar una serie de perspectivas futuras de trabajo. Para finalizar con un apartado donde se detallan los Objetivos. Consta de una Introducción.Estructura de la tesis ESTRUCTURA DE LA TESIS Esta tesis esta organizada manteniendo la estructura de cualquier texto científico. tratando de dar una visión integradora. cinco Capítulos que conforman el cuerpo principal de esta tesis. La Introducción general. en esta tesis doctoral se ha mantenido un mismo formato para todos los capítulos. . INTRODUCCIÓN . . (5) comportamiento influido por el excesivo sol y la escasez de agua. Benton et al. pero la llegada de los modernos sistemas de gestión agraria y la intensificación agrícola (concentraciones parcelarias. 2005). (6) predominio de cantos aéreos durante el cortejo nupcial. 1997). Las pseudoestepas constituyen en Europa el hábitat principal de un grupo de aves representativas de los medios abiertos y con escasa vegetación. la situación ibérica en cuanto a la conservación de estos medios es mucho mejor que la del resto de Europa. excepto en especies de gran tamaño. presentan características morfológicas. junto con el abandono de cultivos durante el último siglo. homogeneización del paisaje. 2001. En España hasta los años 70-80. 2003. La península Ibérica es una de las zonas de Europa Occidental donde las pseudoestepas cerealistas presentan mayor extensión. han modificado la calidad y extensión de hábitat disponible (Chamberlain et al. incluyendo baños de arena. etc. desaparición de lindes.Introducción 1. (4) marcada tendencia al gregarismo. lo que es de vital importancia para la conservación de la biodiversidad europea (Pain & Pienkowski 1997). 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). llegando a ocupar un alto porcentaje de la superficie del continente europeo. fisiológicas y etológicas similares: (1) nidificación en el suelo o cerca. 2005). denominadas genéricamente aves esteparias (Suárez et al. y (7) adaptaciones dirigidas a reducir el impacto de la depredación del nido. Éstas constituyen un conjunto filogenético muy heterogéneo de especies que. 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. lo que a su vez. sin embargo. Aparentemente. estos ecosistemas habían permanecido poco alterados y en un estado estable de conservación. 2001. aumento del regadío. (2) coloración críptica. 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. Bota et al. Donald et al. aumenta el compromiso por su conservación.). ya que es de las áreas que alberga mayores poblaciones de aves esteparias de Europa (Santos & Suárez 5 . 2004. incremento del uso de agroquímicos. 2000. (3) propensión a desplazarse caminando. Bota et al. Brotons et al. Canarias y Madeira). noroeste de Italia. ha sido introducida en Reino Unido. estas mismas zonas constituyen el principal área de caza de perdiz roja en el mundo. tiene un alto valor ecológico. 2004. 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. Vargas et al. 2003). Rueda et al. Blanco-Aguiar 2007). Presenta un característico plumaje. 2. Las perdices no constituyen la especie de presa principal de ningún depredador ibérico. como el águila imperial ibérica (Aquila adalberti) o el lince ibérico (Linx pardinus). y las islas italianas de Elba y Córcega). Portugal. en Estados Unidos. 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. Otro aspecto destacable de su ecología es una alta productividad. Francia. 2003. Además. además de una llamativa coloración roja en anillo periocular. Nueva Zelanda y Europa central (Blanco-Aguiar et al. 2006. a pesar de que se tiene constancia científica de su condición de presa. Está presente en un amplio tipo de hábitats. en al menos alguna 6 . presa clave de la mayoría de los depredadores ibéricos (Calderón 1983). 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). puesta e incubación) cuando presenta un comportamiento más territorial (Cramp & Simmons 1980). junto al conejo de monte (Oryctolagus cuniculus). incrementando la sobreexplotación sus poblaciones (Blanco Aguiar et al. es en estos medios donde alcanza sus mayores densidades (Blanco-Aguiar et al. Además. islas del Atlántico (Azores. Blanco-Aguiar 2007). en numerosas regiones de España la presión cinegética se redirigiera hacia la perdiz. Este papel como presa clave.Fabián Casas Arenas Tesis Doctoral 2005). ya que es. incluyendo varias especies endémicas y/o amenazadas. aunque no es considerada estrictamente esteparia. junto a la aparición de la enfermedad vírica del conejo. en el que destacan principalmente el bandeado de las plumas del costado. especie que. pico y patas. además de una gran importancia como especie de caza menor. desde el nivel del mar hasta los 2500 metros de altitud. con primeras puestas que suelen variar entre 10 y 18 huevos (Cramp & Simmons 1980. y el babero negro de las plumas del cuello. Su distribución natural está restringida a la región mediterránea (España. y con poco éxito. ha podido provocar que. La perdiz roja. que normalmente suele resolverse a favor del hombre. dada su condición de presa para múltiples depredadores y de recurso cinegético para el hombre. para el uso de la tierra de muchos propietarios en varios países europeos como Reino Unido. la caza es una importante actividad económica que genera sustanciales beneficios. 2005). Es ésta una de las principales opciones alternativas o complementarias (agricultura. siendo por tanto. ganadería. 3. habría que añadir su condición de especie endémica de la región mediterránea (Del Hoyo 1994). como es aclamado por la comunidad cinegética. siendo el control de depredadores la herramienta de gestión más utilizada (Arroyo & Beja 2002)..…). Una relación de denso-dependencia podría deberse al carácter oportunista de determinados depredadores como el zorro (Delibes-Mateos et al. 16 mamíferos y 3 reptiles (Yanes et al. la densidad de perdices y sus depredadores. pollo o adulto) para 23 aves. podría ayudar a clarificar hasta qué punto la depredación es importante. Martinez et al. En cualquier caso. Esta actividad tiene un importante valor socioeconómico especialmente en zonas rurales menos favorecidas. le confiere una gran importancia conservacionista. 1998. El estudio del efecto de la depredación en la dinámica de poblaciones de la perdiz roja en el más extendido de sus hábitats. Howard & Carroll 2001. España o Portugal. observación personal). 2008). F. 2002). 7 . no están claros los efectos de la depredación en la dinámica de poblaciones. que a su vez. y esta información debería ser uno de los factores más determinantes a la hora de establecer medidas de gestión adecuadas. existe un conflicto de intereses entre cazadores y depredadores. donde tanto el aprovechamiento cinegético como agrícola son la principal fuente de ingresos (Bernabeu 2000. Francia. Ya que. A todo lo mencionado anteriormente. tratándose de una de las especies más emblemáticas que pueblan nuestros campos. Casas. se desconoce el sentido de las relaciones entre las tasas de depredación. o a la disminución en la densidad y/o detectabilidad del conejo (Ontiveros et al. Importancia socioeconómica de la caza de la perdiz roja En general. una pieza crucial de información para comenzar a solucionar este conflicto entre gestión cinegética y conservación de la biodiversidad (Valkama et al. No obstante.Introducción fase de su ciclo de vida (huevo. 2005). como consecuencia de la gran demanda de piezas y del declive de las poblaciones silvestres (ver más adelante). Blanco-Aguiar et al. guardería. y a la vez de la gestión cinegética. 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.Fabián Casas Arenas Tesis Doctoral Concretamente. En conjunto. su estatus real de conservación es mal conocido debido a la falta de datos precisos (Blanco-Aguiar et al. Su caza es especialmente importante en regiones como Castilla-La Mancha. 2004). licencias. Diversas razones podrían explicar este declive. En España se sueltan anualmente entre 3 y 4. patés. 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). muchas de estas perdices criadas en granja forman parte de otro floreciente negocio. Adicionalmente. principalmente en la hostelería y en la industria conservera (perdices escabechadas. En España. Andalucía y Extremadura (Blanco-Aguiar et al. 2003). Esto contribuye al prolífico negocio de la cría de perdices en cautividad. para consumo humano. Bernabeu 2000).5 millones de perdices al año (Garrido 2002). la caza menor en España (principalmente conejo y perdiz) genera un movimiento económico de unos 210 millones de euros al año (Ayala 1985). Aebischer & Lucio 1997). 4.). otro elemento importante de la economía existente alrededor de la caza de esta galliforme. pero la más importante parece ser la alteración del hábitat. etc. la caza de la perdiz roja es una de las actividades económicas más importantes en multitud de áreas rurales de España (APROCA 1998. es la suelta de perdices procedentes de granja.. munición. 2003. que dan lugar a que alrededor de la caza exista un importante número de personas que dependen directa o indirectamente de ella. que desde los años ochenta ha sufrido un incremento sustancial (Blanco-Aguiar 2007). Potts 1980. etc. particularmente los cambios acontecidos durante las últimas 8 . contando con un arraigo social y cultural únicos. ojeadores. 2004). Además. núcleo central de su distribución y donde se encuentran las poblaciones más importantes (Aebischer & Potts 1994. Lucio 1998. Este montante económico se reparte entre los arrendatarios de tierras. Aebischer & Lucio 1997. Aebischer & Potts 1994. en prensa). hay que tener en cuenta que la perdiz roja es una especie eminentemente mediterránea. junto con la sobreexplotación cinegética de las poblaciones en declive. Así pues. Por tanto. Dicho autor concluyó que la intensificación agrícola. poco se sabe sobre cuales de los múltiples cambios que la modernización en los sistemas de explotación agraria ha producido en el ecosistema. sólo recuperadas recientemente gracias a la generalización de las sueltas. ¿Qué esta ocurriendo realmente con las poblaciones naturales de perdiz roja en los últimos años? Parece claro. Vargas et al. factores que afectan directamente a su productividad anual y mortalidad invernal (Lucio 1990). lo que contrasta con lo expuesto anteriormente. La depredación. y por tanto sometida a una alta variabilidad climatológica interanual y elevada presión cinegética. Recientemente ha sido realizado el primer análisis a largo plazo de las bolsas de caza de perdiz roja en España (Blanco-Aguiar 2007). concretamente durante la década de los 70 (Blanco-Aguiar 2007). y por tanto a las densidades en primavera. que en las últimas décadas ha existido un declive generalizado de sus poblaciones. son los principales factores que explican la disminución en las rentas cinegéticas de perdiz durante las últimas décadas. 2004. no está claro cual es la importancia relativa de este complejo grupo de factores. aunque el programa SACRE desarrollado por SEO/BirdLife aunque ya recoge datos de 9 . podrían ser también importantes. 2004. 2007).Introducción décadas en los modelos de gestión agrarios (Lucio & Purroy 1992. las mejores estimas disponibles sobre tendencias poblacionales de aves comunes en España son las del Programa SACRE de SEO/BirdLife. Villanúa et al. 2003. una posible explicación a esta aparente estabilidad actual sería que las poblaciones se mantengan constantes. Blanco-Aguiar 2007). la sobreexplotación cinegética o problemas asociados a la suelta de perdices procedentes de granjas (introducción de nuevos patógenos o introgresión genética). están detrás del declive de las poblaciones de perdiz roja. No obstante. Vargas & Cardo 1996. Blanco-Aguiar 2007. a tenor de lo acontecido en buena parte del área de distribución de la especie. 2006. 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. Los informes anuales de dicho programa apuntaban una tendencia a la disminución en las poblaciones de perdiz roja. Blanco-Aguiar et al. al menos localmente (Nadal 1992. pero a unas densidades inferiores. Sin embargo. Millán et al. SEO/BirdLife 2006. si bien. Pero aún conociendo esto. Actualmente. 1987a. 2006. Alonso et al. Cabezas-Diaz & Virgos 2007. más si cabe cuando este tipo de información es clave para el desarrollo de medidas de gestión y planes de conservación efectivos. 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. las medidas de gestión más extendidas en los hábitats que ocupa la especie van a ir dirigidas a aumentar el 10 . serían necesarias series más largas para establecer tendencias inequívocas. 1987b. Esto hace todavía más complejo desentramar cuales son los factores que pueden influir en la tendencia poblacional de esta especie. esta liberación masiva de perdices no sólo no ha contribuido a una recuperación de las poblaciones naturales de perdiz roja. 2005. ecológica y conservacionista de la perdiz roja. ésta (al igual que muchas otras especies cinegéticas) puede actuar como especie “paraguas”. 1986. A todo lo anterior. Blanco-Aguiar 2007. Paradójicamente. Medidas de gestión cinegética aplicadas a la mejora de las poblaciones de perdiz Dada la recalcada importancia económica. unas medidas de gestión ineficaces o mal establecidas. a pesar de la mencionada importancia tanto ecológica como socioeconómica de esta especie. social. Villanúa 2007. Aunque recientemente esta tendencia parece estar invirtiéndose con una proliferación de nuevos trabajos sobre diversos aspectos de la biología de la perdiz (Fortuna 2002. Rands 1986. se ha recurrido a las sueltas de perdices procedentes de granja como herramienta de gestión de uso común. Millán 2004. 1988) que sobre la población autóctona ibérica. Vargas et al. Además. 1984b. Pérez-Rodríguez 2007. En cambio. Green 1983. Tapia & Domínguez 2007). 5. Debido a la mayor importancia socio-económica. habría que añadir que el conocimiento de la biología general de la perdiz roja en España es relativamente pobre. aún hay aspectos clave de los que se carece de la suficiente información. 1984a.Fabián Casas Arenas Tesis Doctoral una cantidad considerable de años (1996-2005). pueden producir el efecto contrario. Adicionalmente. si no que se sospecha que la introducción de estos ejemplares incluso ha podido agravar la situación de las poblaciones silvestres (Dowell 1992). tanto para mantener poblaciones cazables como para incrementar el rendimiento económico de las explotaciones cinegéticas. sobre todo de aquellos concernientes a la gestión cinegética. resultaba sorprendente encontrar más información sobre la población de perdiz roja introducida en el Reino Unido (Potts 1980. En cambio. sin lugar a dudas. 2002. especialmente aquellas más sensibles a la depredación de nidos por especies generalistas como zorros (Vulpes vulpes) y urracas (Pica Pica. la gestión del hábitat. que suelen ser el grupo sobre el que se suelen centrar los objetivos de control. Sí es conocido. Entre las medidas de gestión cinegética de más amplio uso destacan el control de depredadores. que un control de depredadores mal realizado puede generar una pérdida de biodiversidad dentro del gremio de los carnívoros terrestres (Virgós & Travaini 2005). el devenir tanto de las poblaciones silvestres de perdiz como de las poblaciones de otras especies con las que comparte el mismo medio. Delibes-Mateos et al. 5. muy posiblemente por la fuerte relación positiva entre costes y beneficios a corto plazo (Díaz 2006). 1996).1. en prensa) y. Ésta última es sin duda la medida de gestión que recientemente esta creciendo en adeptos. incrementando a su vez la densidad poblacional (Tapper et al. la información disponible sobre el efecto de esta práctica de gestión en otras especies diferentes a las cinegéticas es muy escasa (Arroyo & Beja 2002). Este hecho condiciona de forma importante.Introducción rendimiento cinegético de sus poblaciones. Finalmente. aumentando su éxito reproductivo. 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. sobre la dinámica de poblaciones de la perdiz roja. más concretamente. junto con la protección legal de los depredadores y una reducción en la 11 . De Borbón et al. a pesar de la escasez de información que se tiene sobre el efecto de la depredación en estas especies (Herranz et al. se ha demostrado que el control de depredadores puede contribuir a un aumento de su éxito reproductivo. Yanes & Suárez 1996. Sin embargo. 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). Díaz 2006). Por otro lado. sin embargo. para la que existe más información. y son por tanto mucho más generalizadas que las emprendidas para la gestión de otras especies amenazadas. Esta percepción. 1999). otras especies podrían beneficiarse de una disminución en los tamaños poblacionales de los depredadores. la colocación de bebederos y comederos. y la repoblación con perdices procedentes de granja. en otras especies cinegéticas como la perdiz pardilla (Perdix perdix). Fabián Casas Arenas Tesis Doctoral 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 Fabián Casas Arenas Tesis Doctoral 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 Fabián Casas Arenas Tesis Doctoral 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 (BlancoAguiar 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 Fabián Casas Arenas Tesis Doctoral 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 El 19 . Por otro lado. esto puede significar que junto con la gestión agrícola. Sin embargo. 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. y algunos de los posibles efectos que se podrían derivar de tal actividad aún no están bien explorados. en su hábitat principal y donde alcanza mayores densidades. tamaño de puesta y éxito de eclosión) de la perdiz roja (capítulo 1). han extendido el problema a las poblaciones silvestres. poco se sabe sobre los parásitos sanguíneos. Sin embargo. esta información puede resultar de utilidad para otras especies que comparten el mismo hábitat. condición física. Este es un factor importante para determinar la relevancia en el éxito reproductivo de ambos sistemas de gestión. Evaluar las diferencias en tamaño corporal. La suelta de perdices procedentes de granja es un fenómeno muy extendido. 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). Los parásitos intestinales de perdices procedentes de granja y de perdices silvestres difieren sustancialmente. las pseudoestepas ibéricas. Igualmente las sueltas de perdices pueden inducir problemas a nivel sanitario. 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. amenazando la conservación de la pureza genética de la perdiz roja. supervivencia y causas de mortalidad entre híbridos y no híbridos. Por tanto. 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). Por ello. poco se sabe del papel que pueden estar jugando estás perdices híbridas en la naturaleza. en una zona donde el aprovechamiento agrícola no es el único que se obtiene de la tierra. el primer objetivo de esta tesis es conocer los factores que pueden influir en la reproducción (doble puesta. donde la escasez de lugares adecuados para la nidificación de las aves es un factor limitante. parámetros reproductivos.Introducción variabilidad climatológica interanual. Así pues. la gestión cinegética suponga otro de los factores que influyan en el éxito de nidificación de la perdiz roja. la pseudoestepa es un medio sometido a un intenso y continuo manejo del hábitat. Además. Sin embargo. podría ayudar a conocer la magnitud del problema y determinar cuál puede ser la mejor estrategia para solucionarlo. 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. suelen tener bajas prevalencias de parásitos sanguíneos. esto permitiría proponer importantes herramientas para mejorar la gestión agraria que favorezcan. 20 . La suelta de perdices procedentes de granja podría alterar esta estructura espacial. Además. los cambios inducidos por los humanos en el medio ambiente podrían alterar la estructura genética espacial de ambos. tanto a las poblaciones de aves objeto de estudio como a las que comparten su hábitat. gestión de la vida silvestre y biología de la conservación.Fabián Casas Arenas Tesis Doctoral 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. Además. en distintos países de Europa se han establecido una serie de zonas protegidas. La caza es una de las actividades humanas que más afecta a la vida silvestre. etología. Por último. 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). 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. ecología. y que además recibe una creciente atención dada su dimensión social y económica. 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. las especies que habitan medios abiertos como en nuestro caso. parásitos y hospedadores. No obstante. El cuarto objetivo es determinar la prevalencia de los parásitos sanguíneos en una especie habitante de medios pseudoesteparios. parasitología. Con la integración de la información obtenida de los cinco objetivos propuestos. el incremento de las actividades de ocio humanas ha amplificado las potenciales consecuencias de la perturbación humana en la fauna silvestre. donde la caza no esta permitida y que no suelen ocupar más de un 10 % de la superficie del coto de caza. así como los parámetros geográficos y las implicaciones de la gestión cinegética que pudieran condicionar la distribución y presencia de los parásitos (capítulo 4). . Aebischer. Poyser. J. & Lucio. & Dessi-Fulgheri. En: Proceedings of the symposium on the status. Arroyo. (1985) Adecuación y desarrollo de la oferta de caza menor a la demanda turístico-cinegética. & Otero. 208-209. Di Giuseppe. & Potts.. Game Fund Service. Negro. quail and turtle dove in the Mediterranean region. thrush. A. R. C. G.. T. Heath).J.. V. Pérez.M. R. N. Cappelli. British Poultry Science 46. 275–287.F. Birdlife Conservation Series nº3.. pp. Analysis of the genetic Structure of red-legged partridge (Alectoris rufa.J..htm) European Commission. J. 182-188. F.. N. & Dini.D. (2002) Impact of hunting management practices on biodiversity.es/irec/reghab/ informes. M. (eds W. incidencia y causas. and conservation of the species Alectoris..J. Their Conservation Status. Córdoba. J. T & A. Londres. España. Chipre.Introducción BIBLIOGRAFÍA ADENA. Ayala. G. (2003) Farmland biodiversity: is habitat heterogeneity the key?. Bruselas. Diéz. D. Bernabeu. Blair). Vickery. C.R. M. Birdlife International. management.G.uclm. En: Birds in Europe. (2001) Status y perspectivas de la perdiz roja en España. (1997) Red-legged Partridge Alectoris rufa. B. (2006) El veneno en España (1990-2005). Aebischer. Prieto. F.M. (2005) Study of survival. Ammannati. (http://www. 21 . 29–35. Bertoncini. J. 214-215. Pp: 93-106. Nicosia. (eds G. F. Tucker & M. (2000) Evaluación económica de la caza en Castilla-La Mancha.A. Ministerio del Interior. Madrid. Cambridge. (1998) Valoración económica de la caza en la provincia de Ciudad Real. Barbanera.J. 96-110. Report WP2 to REGHAB project. Gaudioso. (2004) Introgression of chukar genes into a reintroduced red-legged partridge (Alectoris rufa) population in central Italy. Trends in Ecology and Evolution 18. Hagemeijer & M. Ciudad Real. Animal Genetics 36.A. APROCA. F. Galliformes) populations by means of mitochondrial DNA and RAPD markers: a study from central Italy. pp. 401–406. pp.. R. Tesis doctoral. Alonso M.R.J. black francolin.E. F. (2005).. En: The EBCC Atlas of European Breeding Birds: Their Distribution and Abundance. J. Magnelli. Baragaño. Baratti. Universidad de Castilla-La Mancha.L. Benton.. Análisis del problema.R. En: Segundas Jornadas de Turismo Cinegético. Biological Conservation 122. ADENA. C. Reino Unido. P. & Beja. dispersal and home range of autumn-released red-legged partridges (Alectoris rufa). Propuestas de WWF/Adena. (1994) Red–legged partridge. & Wilson. En: La caza en la provincia de Ciudad Real. R. J. Atienza). C. Mañosa. (eds. R. P. M. 771-788. & Villafuerte. Bota. 620-625.B. E. (2001) Análisis preliminar del estatus del sisón en Castilla-La Mancha y posibilidades de programas agroambientales de conservación. pp. Bunce. XVIII Congreso español y III Ibérico de ornitología. R.).. & Virgos.. 182-185.. Madrid. & Estrada.. Biodiversity and Conservation 13. Borralho..M..A. Del Moral). E. Elche (Alicante). S. & Viñuela.L.. 4eme Seminaire international sur l’outarde canepetière. España. Virgós. Madroño.Fabián Casas Arenas Tesis Doctoral Blanco-Aguiar.. Ruiz-Peinado. Universidad Complutense de Madrid. En: Libro Rojo de las Aves de España. Virgós. G. Barcelona.G. Tesis Doctoral. S.. Simoes. R.H. M. González.A. J. L. Universidad Complutense de Madrid. Rego. J. Mañosa. Aspectos morfológicos. España. & Villafuerte..E.A. (2000) Changes in the abundance of farmland birds in relation to the timing of agricultural intensification in England and Wales.M... Castuela. J. España. Cabezas-Diaz.. & Viñuela. Ardea 95. Moraleda. E. D. 22 . Lynx edicions & Centre Tecnològic Forestal de Catalunya.. (2007) Adaptive and non-adaptive explanations for hatching failure in eggs of the red-legged partridge Alectoris rufa. F. Dirección General de Conservación de la Naturaleza y Sociedad Española de Ornitología. J. L. Duckworth. (2005) Ecology and conservation of steppe-land birds. (1998) Summer distribution of Red-legged Partridges Alectoris rufa in relation to water availability on Mediterranean farmland. J. Dirección General para la Biodiversidad-SEO/BirdLife. España. taxonómicos y biológicos. J. J.. J. J.. Tesis Doctoral.C. 5563. (2004) Perdiz Roja (Alectoris rufa). S. Blanco-Aguiar. (1983) La perdiz roja. España. González & J. (2004) Modelling the effects of irrigation schemes on the distribution of steppe birds in Mediterranean farmland. J.A. A. Journal of Applied Ecology 37. España.. Alectoris rufa (L.V. Bautista. Fuller. H. pp. (eds. E. Martí & J. Casas. J. Carrasco. A. Virgós. Blanco-Aguiar. 1039-1058. Rito.V. Blanco-Aguiar.C. J. Calderón.C. En: Atlas de las aves reproductoras de España. (2006) Especies que comparten el uso de los bebederos de perdiz roja (Alectoris rufa). 212-213. (2007) Variación espacial en la biología de la perdiz roja (Alectoris rufa): una aproximación multidisciplinar. Brotons. & Camprodon. F.J.. Madrid. Chamberlain. Morales. Guzmán. R. (2003) Perdiz Roja (Alectoris rufa). Ibis 140. & Pinto. J. R. J. & Shrubb. European Journal of Wildlife Research 54. Elliott. pp 25-48. Donald. J.N. Del Hoyo. R. Woodburn. S.. Lynx edicions & Centre Tecnològic Forestal de Catalunya. (2005) Effects of spring supplementary feeding on population density and breeding success of released pheasants Phasianus colchicus in Britain. Gibier Faune Sauvage 9. (2002) Spring body condition of hen pheasants Phasianus colchicus in Great Britain. Barros.I. (1999) Parámetros reproductivos de la Ganga Ibérica (Pterocles alchata) y la Ganga Ortega (Pterocles orientalis).. Lynx Ed.E. biología y conservación.. E. E. M. J. Oxford University Press. & Heath. M.A. R. Proyecto fin de carrera de Ingeniería de Montes de la Universidad de Valladolid.. Wildlife Biology 11. (en prensa) Rabbit populations and game management: the situation after 15 years of rabbit haemorrhagic disease in central-southern Spain..H. España.. Palencia. Biodiversity and Conservation DOI 10.. 71-78. A. (2006) Caracterización de la gestión cinegética y agraria en cotos de caza menor de la Comarca de Montiel (Albacete) y evaluación de su influencia en las capturas de perdiz roja (Alectoris rufa). Green. P. D.H. J. Oxford. J.. De Borbón. Delibes-Mateos. (2008) Feeding responses of the red fox (Vulpes vulpes) to different wild rabbit (Oryctolagus cuniculus) densities: a regional approach. Wildlife Biology 8.L. 261-266.Introducción Cramp. 177-182.B.P. De Juana.F. Proceedings of the Royal Society of London Series B 268. & Camprodon. Organismo Autónomo Parques Nacionales. De Juana. P. Draycott... R.). Bota. P. & Herránz. España.M. Ministerio de Medio Ambiente. J. K.1007/s10531007-9272-5. 25-29. (1980) The Birds of the Western Palearctic. & Sage. II. J.D. M. & Carroll. S. (1992) Problems and pitfalls of gamebird reintroduction and restocking: an overview. Mañosa. Delibes-Mateos. Dowell. S. & Villafuerte. G. & Simmons.A. M. Vol.F..B. & Sargatal. Vol. 773-780. Barcelona. M. En Herranz & Suárez (eds.I.. M. Morales. 23 . & Ferreras. II.B. R. Villafuerte.A. abundancia. Carroll.E. R. Parish. Draycott. (1994) Handbook of the Birds of the World. (2005) Steppe birds: a characterisation.P... R. Díaz. (2001) Agricultural intensification and the collapse of Europe’s farmland bird populations. Ferreras. S. Woodburn. En: Ecology and conservation of steppe-land birds (eds. J. M. Guadalfajara.): La Ganga Ibérica (Pterocles alchata) y la Ganga Ortega (Pterocles orientalis) en España: Distribución..A. Barcelona. R. C. Fernandez de Simón. (1999) Effects of supplementary feeding on territoriality. tomo I. Revista Ibérica de Parasitología 42. Green.E. (2000) Success of traditional restocking of red-legged partridge for hunting purposes in areas of low density of northeast Spain Aragón. R. & Suárez. J. 24 . 59-66. A. J.H.E. Spring Dispersal and Agonistic Behaviour of the Red-Legged Partridge (Alectoris-Rufa). A.. (1983). Lucio & M. Game and Wildlife Science 21. Ardeola 49. Duriez. Draycott. M. C.Fabián Casas Arenas Tesis Doctoral Duarte. (1984a) Double nesting of the red-legged partridge Alectoris rufa. Pp. Green. pp. Green. Garrido. Zeitschrift fur Jagdwissenschaft 46. Eraud. & Ferrand. breeding success and survival of pheasants. Journal of Applied Ecology 21. (2004) Field interbreeding of released farm-reared Redlegged partridges (Alectoris rufa) with wild ones.. (2001) Driven game shooting on farms in Essex. A. Journal of Applied Ecology 36.L. FEDENCE-EEC. Aportaciones a la gestión sostenible de la caza. 157-169. J. Ibis 126. 1-13.. R. En: Aportaciones a la gestión sostenible de la caza.N. Hoodless. & Robertson. M. Howard. 817-830. 541-555. & Carroll. Ludiman. F.. (2002) El impacto de la prelación sobre las poblaciones de perdiz roja.M. & Vargas..D. FEDENCA. Y. 147-156.A. Yanes. 332-346. Journal of Applied Ecology 34.E. (2005) Factors affecting population dynamics of Eurasian woodcocks wintering in France: assessing the efficiency of a hunting-free reserve. 141-147. O. R. (2002) Capturas de perdiz roja (Economía inducida por la caza de perdiz). J. Herranz. UK: Implications of land management and conservation. C. (1982) Plasmodium relictum y P. M.A. Barbraud. cathemerium en Aves del área salmantina. J. Fox. (eds. 89-97. Journal of Zoology 201. M. 55-61. 81-100. N.N. & Madsen J. Fortuna. Villafuerte. A. R.A. 23-30. Biological Conservation 122. 269-306. Madrid. (1984b) The Feeding Ecology and Survival of Partridge Chicks (AlectorisRufa and Perdix-Perdix) on Arable Farmland in East Anglia.. P. Game & Wildlife Science 18. R. (2002) Selección de hábitat de la perdiz roja Alectoris rufa en período reproductor en relación con las características del paisaje de un agrosistema de La Mancha (España). & Martín. Gortázar. Encinas. (1997) Behavioural and distributional effects of hunting disturbance on waterbirds in Europe: implications for refuge design. C. Madrid. Sáenz de Buruaga). M.J.K. Earle. Academic Press. Little. Brooke. EE.. Gestión del Hábitat. 63-92. 25 . Lucio. (2004) A comparison of the helminth faunas of wild and farm-reared red-legged partridges. Biological Conservation 98: 19-24. Ardeola 37. (1998) Recuperación y gestión de la perdiz roja en España. Pp. caza y vida silvestre.J. Nadal. (1990) Influencia de las condiciones climáticas en la productividad de la perdiz roja (Alectoris rufa). San Diego. Lucio. Millán. Gortázar. R. 87-100. (2005) Correlates of extinction risk and hunting pressure in gamebirds (Galliformes). (1992) Caza y conservación en España. 193-207. Bélgica. Nadal. Bruselas. (1992) Problemática de las poblaciones de perdiz roja. (1995) Sandgrouse (Pterocleidae) and sociable weavers Philetarius socius lack avian Haematozoa in semi-arid regions of South Africa. Biological Conservation 126. 85-98. FEDENCA. Negro. A. España.J. R. J. J.. M.. Barcelona. I. J. C. J. Martínez. (2001) RAPD analysis for detection and eradication of hybrid partridges (Alectoris rufa x A-graeca) in Spain. (2002) Socioeconomic and cultural aspects of gamebird hunting. A. de L. J. 207-218. bases ecoetológicas para tener éxito con las repoblaciones.. 701-707. Madsen. (1995) Impacts of hunting disturbance on waterbirds-A review.Introducción Keane. R. (eds. Ardeola 39. Universidad de Zaragoza. Torres. R. Madrid. F. J.) (1994) Predación. I curso. (coord. A. Journal of Wildlife Management 68. A. J. R. 3345. & Villafuerte. Nadal. 216– 233. (2004) Alteraciones asociadas a la cría en cautividad de Galliformes silvestres.A. (1998) Population limitation in birds. pp. M.J. Gortázar.J. P. J. Newton. Journal of Arid Environments 30. Sáenz de Buruaga). P. La Perdiz Roja. (2003) Does supplementary feeding affect organ and gut size of wild red-legged partridges Alectoris rufa? Wildlife Biology 9. Millán. España. J. Wildlife biology 1 (3).J. European Commission. pp. & Mcgowan. Madrid. Viñuela. & Fox. En: La perdiz roja. & Villafuerte. Tesis Doctoral. 367–370.A. & Purroy. 229-233.J. AedosFundación “La Caixa”. La perdiz roja. & Comalrena. Lucio. Fundación La Caixa. J. Barcelona.M. Grupo Editorial V-FEDENCA.. (1998) La Bioecología de la perdiz roja. C. Millán. REGHAB project.D. A. España. & Villafuerte. J. & Godoy.UU. R. Journal of Applied Ecology 23.W. testosterona y carotenoides. (1980) The effects of modern agriculture.R. 882-888. G..A. & Sotherton. The Common Agricultural Policy and its implications for bird conservation. M. (2007) Señales fiables en la perdiz roja (Alectoris rufa): condición física. Biological conservation.R.. J. 2-79.B..J. 35-40.W. L. Robinson. 397-408.R. (2004) Game crops and threatened farmland songbirds in Scotland: a step towards halting population declines? Bird Study 51. Bulletin Mensual Office Nacional de la Chasse 184. & Notario. (1986) Effect of Hedgerow Characteristics on Partridge Breeding Densities. 2-9. (1986) The partridge. & Bennett. Journal of Zoology 212.G. Pesticides.M. Rands. Academic Press. G. Ecological Research 2. M. J. D. (2004) Use of radiotracking techniques to study a summer repopulation with red-legged partridge (Alectoris rufa) chicks.A. Rueda.Fabián Casas Arenas Tesis Doctoral Ontiveros. J. D. (2004) Having your wildlife and eating it too: an analysis of hunting sustainability across tropical ecosystems. Díez. M. M. Ornis Scandinavica 19. London. Potts. Animal Conservation 7. E.R.W. (1997) Farming and birds in Europe. & Bartolomé. Alonso. Baragaño. Biological Conservation 40. 123: 19-25. (1988) The effect of nest site selection on nest predation in Grey Partridge Perdix perdix and Red-legged partridge Alectoris rufa.. William Collins Sons and Co. prey detectability and food habits: the case of Bonelli’s eagle and the conservation measures. Universidad de Castilla La Mancha. J. 479-87.R. Pérez. Tesis Doctoral. Rands. (1993) Nidification de la perdrix rouge (Alectoris rufa) dans la région de La Mancha (Espagne). nest predation and game management on the population ecology of partridges (Perdix perdix and Alectoris rufa). Pérez-Rodríguez. España. D. & Pienkowski.W. V.L. J. UK. 26 . London.. 407-418. Potts. 107-112. N. Rands.. predation and conservation..W. (1987a) Hedgerow management for the conservation of partridges Perdix perdix and Alectoris rufa. M. Olmedo.R. Rands.E. & Pleguezuelos.R. A. M. M. Pain D. Caro. Parish.M. Gaudioso. C.W.J. Poultry Science 83. J. (2005) Prey density. (1987b) Recruitment of grey and red-legged partridges (Perdix perdix and Alectoris rufa) in relation to population density and habitat. 127-139. .. Knops J. P. Tapper.W. (2005) Songbirds using crops planted on farmland as cover for game birds. & Camprodon. Morales. S. Mielke. & Suárez. SEO/BirdLife. T. Woodburn. 435-449.T. M. A.. Mañosa.. Monteagudo. (1999) A Question of Balance. Potts. Hadjisterkotis. Academic Press. European Journal of Wildlife Research 53. Parish. Broad-scale habitat use by red-legged partridge (Alectoris rufa) in a low-density area in northwestern Spain. & Brockless.. M. F. eds.. & Le Maho. Fordingbridge. The Game Conservancy Trust. (2007) Introgression of Alectoris chukar Genes into a Spanish Wild Alectoris rufa Population. Lynx Edicions & Centre Tecnològic Forestal de Catalunya. & Lehman.G. Madrid. S.R. (2007). & Thompson. Jarry. & Pienkowski. SEO/BirdLife (2007) Seguimiento de las aves comunes reproductoras en España: Programa SACRE. Stoate. & Domínguez.C. Stoate. (2005) Biogeography and population trends of Iberian steppe birds. C.L. & Arruga M. Madrid.I. 203-209. 843-845. España.) pp 297-330. 27 .. (1997) Farming in the drylands of Spain: birds of the pseudosteppes. SEO/BirdLife. L.V. Barcelona. Hampshire. J. (2004) Development of an agrienvironment scheme option: seed-bearing crops for farmland birds. Informe 1996-2005. M. Bechet. Lefeuvre.V. J. I. 279-292. 248-253. Tapia. En: Farming and birds in Europe. Y.. Londres..B. E.Introducción Sage. A review of literature.B. Mautner. E. Naveso. (2001) Could game management have a role in the conservation of farmland passerines? A case study from a Leicestershire farm.). pp 69-102. J.B. En: Ecology and conservation of steppe-land birds (eds. Tejedor. Journal of Heredity 98. (Pain. & Szczur. & Parish. Tapper. G. Tamisier. (1996) The effect of an experimental reduction in predation pressure on the breeding success and population density of grey partridges Perdix perdix.. Ibis 146 (Suppl. & de Juana. L. Suárez.. Reich PB. J. M.. D. Henderson. Wedin D. S. C. F. Journal of Applied Ecology 33. M. Revue d ecologie-la terre et la vie 58. (2003) Effects of hunting disturbance on waterbirds. Bird Study 42. Informe 1996-2004. Science 294. S. Tilman D. 178-182. 179-182. G. A.G.H. European Journal of Wildlife Research 51. C.C. T.B.A. D. Santos. M. R.. SEO/BirdLife (2006) Seguimiento de las aves comunes reproductoras en España: Programa SACRE. 96-978.M. (2001) Diversity and productivity in a long-term grassland experiment. D.A. Bota. G. 2).M. Acevedo. Casas. Viñuela. Gortázar. Trofeo 317.G. Birdlife International.. Londres. & Cardo. 28 . G. (2007a) First occurence of Eucoleus contortus in a little bustard Tetrax tetrax. R. Kenward. Thirgood.A.B. A. (2007) Parásitos de la perdiz roja (Alectoris rufa): implicaciones para su aprovechamiento cinegético y conservación. Reino Unido. (2005) Birds of prey as limiting factors of gamebird populations in Europe: a review. & Laird. J. F.. J. Thompson. C.C.101–103 Villanúa. E. Arroyo.. Beja. Guerrero. C. M. Redpath. E. & Heath. R. & Gortázar.M.. Fielding. Casas. S. Villanúa. M. M.M. (1996) El declive de la perdiz roja en el olivar. U. (1994) Birds in Europe: their conservation status. & Travaini. (1986) The epizootiology and ecological significant of malaria in Hawaiian land birds. Farfán. Mañosa..G. J.. Universidad de Castilla La Mancha. V. E.1007/s10344-007-0130-2. C... J. Biodiversity and Conservation 14. J. Acevedo. 327-344. Fernandez-de-Mera. C. (2003) Predators and rabbits in Spain: a key conflict for European raptor conservation. M. (2006) Land use and environmental factors affecting red-legged partridge (Alectoris rufa) hunting yields in southern Spain. 188–195. & Gortázar. Biological Reviews 80. Vicente. M. M... van Riper. Bro. J. A negative effect of red-legged partridge Alectoris rufa releases on steppe bird conservation?.Fabián Casas Arenas Tesis Doctoral Tucker.A.. Viñuela. Tesis Doctoral... V. Barral.. Morales.M. S.. Villanúa. 405-406. O. R. Barbosa.. C. S. D. S... J. Rodríguez. Pérez-Rodríguez. Alzaga. P. pp.M. García de la Morena. L. Marquiss & C. M. 23-27. D.. Juste. E. Valkama.. B. van Riper. D. Birds of prey in a changing environment. Ibis 149.. The Stationary Office. Ecological monographs 56. J.M.. (2007b) How effective is pre-release nematode control in farm reared red-legged partridges (Alectoris rufa)? Journal of Helmithology 81. M. Pérez-Rodríguez. S. Bretagnolle. Korpimäki. Veterinary Research 38: 451-464..F. Vargas. J.B. J. J. & Real. A. D. Garrido. R.L. Viñuela. European Journal of Wildlife Research. Höfle. 3475– 3486.M. European Journal of Wildlife Research 52. D.. Cambridge... & Gortazar.. (en prensa) Sanitary risks of red-legged partridge releases: introduction of parasites. 171-203. & Villafuerte.M. Galbraith). Goff. (2007) Risk factors associated with the prevalence of tuberculosis-like lesions in fenced wild boar and red deer in south central Spain. 511-526.. Vargas. L. P. (eds. F. España. (2005) Relationship between small-game hunting and carnivore diversity in central Spain. Redpath. Virgós. P. Villanúa. & Viñuela.L. A. Viñuela. I.... DOI 10. M. Herranz. de la Puente. La Perdiz Roja. & Suárez F. (1998) La Perdiz Roja. Identidad de los depredadores e intensidad de la depredación. J. Grupo Editorial V-FEDENCA. F. Yanes.E. Condor 70. Yanes. pp.. J. (coord.Introducción Warner. Ardeola 43. Madrid. M.. I curso. 29 . R. 101-120. y Suárez. 57-68. Sáenz de Buruaga). M. (1968) The role of introduced diseases in the extinction of the endemic Hawaiian avifauna. (1996) Mortalidad en nido y viabilidad poblacional de aláudidos. 135-147. . and hatching success in wild red-legged partridges Alectoris rufa: novel insights into a peculiar avian breeding system. F. J. . Mougeot.CAPÍTULO 1 Doble incubación. F. en evaluación. 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. & Viñuela. clutch size variation. Double brooding. Behavioural Ecology. . Clutches that were laid late and incubated by males had a lower hatching success. 3. Laying occurred earlier in 2003 than in other years. where partridges achieve their highest densities. The red-legged partridge Alectoris rufa is a game bird with high productivity exhibiting a peculiar breeding system of double nesting behaviour. and males contributed more to incubation in those years. Variation in laying date was explained by year and by the sex of the bird incubating. Hatching success was lowest in 2007. and how these relate to the sex of the incubating bird. The probability of a clutch being lost to predators differed between sexes. similarly so in both sexes. Regulation of clutch size and hatching success could determine the viability of a double clutching behaviour or male uni-parental care systems. a critical information to understand this breeding system that has not been provided up to now. the “agrarian pseudosteppes”. 2. and smallest in 2005. The evolution and regulation of offspring number. Synthesis and applications. Clutch sizes varied significantly among years and between sexes. Females often lay eggs in two different nests. and in its most important habitat. hatching success and the main factors affecting double brooding occurrence. We also examine the factors affecting clutch size and hatching success. depending on year. and breeding systems is a classical study area in ecology that has received major attention in the literature. The main aim of this study was to collect data on the breeding ecology of red-legged partridges in central Spain. one incubated by the female. Females showed similar incubation rate all study years. Females laid more eggs in years when spring rainfall was high. the year when laying was more delayed. most likely more influenced by inter-annual variations in weather conditions and food availability. being higher for nests incubated by females. but later in 2004. parental care. and the other one by its male. This effect was mainly due to year 2005. in the core area of the species. laying date. Clutch size also decreased with increasing laying date. The probability of incubating significantly differed between sexes. In a dry year. clutch size. Average clutch sizes were largest in 2003 and 2007. 4. Variation in hatching success was explained by year and sex. year and hunting management models. 6. 33 . We failed to found differences in all the breeding patterns explored among hunting management models. males do not incubate. with contrasting environmental conditions. This study is the first performed in a long series of years. when no male incubated. Double brooding behaviour could be considered an intermediate stage in the evolutionary trend from biparental to uniparental care of single clutches. allowing an examination of the factors affecting the occurrence and success of double clutching behaviour. Clutches incubated by males were laid earlier than those incubated by females in this year of early laying. 5. the simplest explanation is the lack of effect of hunting management in the breeding ecology of partridges. Clutches incubated by males were larger than those incubated by females. We discuss our results within the context of the evolutionary origin of uni-parental care in birds.Capítulo 1 ABSTRACT 1. but only the proportion of males that incubated varied markedly between years. depending on the ancestral state in the phylogeny). the male caring a first clutch while his mate lays a second one without mate guarding (Pierce & Lifjeld 1998). females are the sex devoting more investment to offspring rearing. Cockburn 2006). Thus. parental care. 1 %.or female-only uniparental care of single clutches (or viceversa. but double brooding is a system apparently requiring “mutual confidence” of sexes. 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. although females are usually the sex devoting more investment (Lack 1968. Clutton-Brock 1991. Cockburn 2006). Reynolds et al. or the female trusting that her mate is going to incubate a clutch instead of deserting and looking for new mates (Green 1984).Fabián Casas Arenas Tesis Doctoral INTRODUCTION The evolution and regulation of offspring number. For example. males are the main providers of parental investment. 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. In most endotherm animals with internal fertilization. Winkler & Walters 1983. 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. An intriguing exception to the general rule of higher female investment is also found among birds. Owens 2002. This system could be considered an intermediate stage in the evolutionary trend from biparental care of single clutches to male. Ligon 1999. The discussion about the origin of uniparental breeding systems is often based on “which sex deserts the other at the nest” (Owens 2002). Green 1984). Ligon 1999). since in a small group of species (c. 34 . Clutton-Brock 1991. and breeding systems is a classical study area in ecology that has received major attention in the literature (Skutch 1982. the most common evolutionary transition detected by phylogenetic analyses (Owens 2002. Martin 1987. mainly precocial species within ratites and charadriforms). Cockburn 2006). 2002. Birds are an exception. taking charge of incubation and post-hatching chick care (Lack 1968. since about 80 % of species provide biparental care to offspring. Cockburn 2006). often without any help by her mates (Clutton-Brock 1991). such as the regulation of clutch size (Green 1984. Cutton-Brock 1991. such as foraging or attracting additional mates (Reid et al. 1999). and when both clutches are laid. Females lay eggs in two different nests. 2002). Ligon 1999. 1994). as a main trait determining fitness. Clutch size variation has long been attributed to food limitation rather than to nest predation in northern temperate climates birds (Roff 1992). Finally. Green 1984). 1993. but EPPs cases of polyginy have been recently documented (Casas et al. but is only common in the red-legged partridge (Cramp & Simmons 1980. 2006b). contrary to Lack’s predictions (Lack 1947). as well as a high divorce rate and frequent mate change during early breeding season (Mougeot et al. due to early feeding autonomy of chicks. Precocial birds such as the redlegged partridge Alectoris rufa have relatively minor reproductive costs as compared to altricial species. and it has been questioned why no more species exhibit a double clutching behaviour (Green 1984). is another contentious issue in evolutionary ecology. or to the origin of uniparental male care breeding systems. Owens 2002). The red-legged partridge is a game bird with high productivity exhibiting a peculiar breeding system of double nesting behaviour (Cramp & Simmons 1980. but also that there may exists a trade-off between parental investment in reproduction and self-maintenance (Clutton-Brock 1991). Male incubation behaviour varies among species of the genera Alectoris. in prep. It is already clear that birds can rear more young than the number of eggs they lay (Monaghan & Nager 1997). This breeding system may be shaped by a complex pool of trade-offs in male and female behaviour. Galliforms in general are among the birds able to lay a higher number of eggs within a breeding season (Lack 1968). Green 1984) and little is known about this breeding strategy. Time spent incubating may reduce the opportunity for males to obtain additional mates or extra-pair copulations (EPC). a basic functional link between double brooding behaviour and clutch size is hatching success. although predation may explain clutch size variation within latitudes (Martin & Clobert 1996). Extrapair paternity (EPP) rates are generally low in species where males contribute extensively to incubation (Schwagmeyer et al. and thus viability of a double clutching behaviour or male uni-parental care systems (Fernández & Reboreda 2007). The 35 . Incubating males would restrict their time available for other activities. Vavalekas et al.Capítulo 1 Intimately linked to the problem of double clutching behaviour. females usually start incubation the second and males incubate the first-laid clutch (Green 1984). Smith & Hardling 2000. Red-legged partridges are often considered as socially monogamous (Del Hoyo et al.). (Green 1984.Fabián Casas Arenas Tesis Doctoral traditional assignment of red-legged partridge to monogamy probably has not been based on rigorous research. 1990. Owens 2002). population density and sex-ratio influencing opportunities for EPPs. Owens 2002. Griffith et al. 2002. attraction of new mates and engagement on EPPs (e. it is important to consider that male incubation could be intimately tied to the physiological ability of females to lay two clutches. The parameters determining why a male takes one way or another could be several. Furthermore. 2002). Potts 1980). Thus. and a period of high predation risk for adults (e. such as breeding status (mated. 2003). Nest abandonment may be relatively common in red-legged partridges (Green 1984. In this context of a complex mating system. mate quality. Cordero et al. a critical information to understand this breeding system that has not been provided up to now. with contrasting environmental conditions. body condition. 2001. what could be the origin of female uni-parental care systems. paternal investment in incubation could affect future survival. Blomqvist et al. divorced or single). Fernández & Reboreda 2003). Females may be particularly exposed to the problem of abandonment by males after copulation (Owens 2002). which might reflect intense mate guarding rather than real monogamy (Westneat et al. but on the common observations of apparently tight social association between sexes. and it is considered a key trait to explain variation in breeding systems of birds (Owens & Bennett 1997. 2002. incubating and rearing chicks or attracting additional females. 1993). Veiga et al. However.g. laying date. 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. males would face a trade-off between paternal investment. females take a risk of loosing their investment when leaving a clutch under the care of their mates. Clutton-Brock 1991. Cockburn 2006). with special reference to the factors influencing double clutching behaviour. allowing an examination of the factors affecting prevalence and success of double clutching behaviour. males could follow two kinds of strategies. It has been shown that the costs of breeding for males taking charge of clutches in precocial species can be high (Holt et al.g. It is obvious that laying eggs in two different nests is a female decision at the root of the double brooding strategy. since incubation may commonly be a period of time and energy limitation in birds (Deeming 2002). the study was performed at the core area of the species and in its most 36 . The main aim of this study was to collect data of the breeding ecology of redlegged partridges in central Spain. Rueda et al. Additionally. Therefore. we used cage traps with adult alive partridges inside the cages as a decoy to 37 . Natural vegetation areas are very scarce. and how these relate to sex. year and hunting management models. and urban areas (mainly country houses) cover less than 10% of the area. radio-tracking and nest monitoring We conducted the fieldwork in 2003-2005 and in 2007.Capítulo 1 important habitat. with interspersed patches of olive groves. Data Collection Captures. 38º 80´ N. vineyards. laying beginning date. we caught 135 adult partridges in February-March (39 in 2003. including just some small areas of short scrubland and pastureland mainly limited to the rocky top of hills. clutch size and hatching success.s. Furthermore. ploughed or abandoned farmland. mainly cereal (particularly barley). We discuss our results within the context of the evolutionary origin of uni-parental care. in spring and early summer (February to June). 2006). 3º 80´ W. characterised by three different hunting management models (hereafter “sites”. MATERIAL AND METHODS Study area The study area covered 125 km² and was located in Campo of Calatrava (Central Spain. The study area included four game estates. 32 in 2005 and 44 in 2007). We examine the factors affecting double clutching occurrence. Over the four years. Vargas et al. where partridges achieve their highest densities (Blanco-Aguiar et al. and a few patches of dry annual legume crops (mainly vetch Vicia sativa) and sugar beet Beta rubra.). 2003. the red-legged partridge is a game bird with high socioeconomic value. This is an undulated farmland area dominated by a mosaic of crops. Other crops.l. 610 m a. and research on factors regulating breeding ecology in natural populations may help managers to develop management tools for improving productivity. the “agrarian pseudosteppes”. while the most important work performed up to now was conducted on an introduced population established in a sub-optimal area (Green 1984). see chapter 2 and 4). For the period 2003-2005. 44 in 2004. This was done either from (1) daily radio-tracking allowing us to determine the exact day when incubation began (in 2003-2005. Year. Del Hoyo et al. Cabezas-Díaz & Virgós 2007). Each bird was fitted with a necklace radio-transmitter with mortality sensor (BIOTRACK. In 2007. when nests were visited during hatching or when the day the radio-tagged bird left the nest with recently hatched chicks was known. we located birds every 1-5 days by radio-tracking. excluding replacement clutches (n=5). 10 gr. nest separation distance. and released at the capture site. and most nests in 2007). All captured birds were sexed from plumage. Madrid. Traps were baited with wheat to attract partridges. birds were caught at night. or (2) by estimating the day incubation started from egg density (some nests in 2007. unpublished data). We also took a blood sample from the brachial vein (0. using AOR-AR8200 multiband receptors and three element YAGI antennas.5-1 ml) to confirm the sex of birds using genetic analyses of blood samples (authors. clutch size and incubation beginning date (1= 1st April) of radiomarked pairs of Red-legged partridges with two nests simultaneously active.). 2001). and estimated for how many days eggs had been incubated given their measured density during the nest visit. Spain). Pair 1 2 3 4 Year 2004 2007 2007 2007 Nest Separation (m) 76 381 314 96 Clutch Size Male 12 14 17 16 Female 10 11 12 14 Incubation Beginning Date Male Female 53 43 43 37 47 41 61 40 38 . or (3) backdating from known hatching date (considering that incubation lasts 24 days and that it starts after laying of the last egg. 1994. we established the daily egg density loss of incubated eggs. After capture.Fabián Casas Arenas Tesis Doctoral catch partridges. by lamping and netting them with a hand-held net. Table 1. biometry and ornaments (Sáenz de Buruaga et al. when birds were found on several consecutive days at the same location. and by locating roosting birds with a powerful head-torch or using an infra-red camera (Panatec. unpublished data). We first determined for each nest the onset of incubation (± 2 days). All analyses were carried out exclusively with first clutches. We located and visited nests using radio-tracking. In 2007. and the other by herself (Green 1981. with the dependent variable “incubation” (0=no incubation. so we estimated laying dates as the day incubation started. minus the final clutch size multiplied by 2 days. one incubated by his mate. we performed a second GLMz analysis for each sex separately. independently of final nest fate. with year and sites as independent variables following the same procedure. the capture method (cage traps). 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. 1=incubation). defined as the percentage of radio-tagged individuals of each sex that began to incubate a nest. we calculated a “nest incubation rate”. Statistical Analysis Differences in incubation rate between the sexes Female red-legged partridges may lay two clutches. Model fitting was assessed by Akaike’s Information Criterion (Burnham & Anderson 1992). usually two. and the level of significance was established at 5 %. Individuals that died before incubation (n =22 females. 1984). improving our success (18 complete pairs caught). because they may lay eggs in more than one nest. The only way to precisely determine the overall number of eggs laid by a female is monitoring simultaneously both members of the pair. was little successful for catching both pair members (16 complete pairs caught). Clutch size Determination of overall clutch size of female red-legged partridges is a difficult task. and sex as explanatory variables. We determined hatching success by visiting nests soon after hatching was detected (1-2 days). Bearing this in mind. After detecting differences between sexes. the first usually incubated by the male and the second by herself (Green 1984). subsequently following a backward stepwise procedure (Crawley 1993). we changed the capture method. n =18 males) were excluded from these analyses.Capítulo 1 Females lay eggs every two days on average (Cabezas-Díaz & Virgós 2007). Even so 39 . From 2003 to 2005. Laying dates were indexed relative to the 1st of March (day 1). we excluded from our analyses clutch losses due to agricultural practices (n = 13) or poaching (n = 3). b). and followed the same procedure described above. we also know that intraspecific nest parasitism or polygamy is relatively common in this species (Casas et al. and date of laying onset. laying beginning date was encoded as to March 1 equal to day 1 for all study years. considering “clutch size” as a continuous dependent variable. in preparation). We explored the sources of variation in clutch size by using a General Linear Model (GLM) with normal error function and identity link function. 40 . the energy requirements increase with increasing clutch size (Ward 1996. and the unbalanced sample sizes among sites. excluding cases in which the clutch was lost during laying or in which the final clutch size was not recorded. We initially included all remaining two-way interactions. In this subsample. given that our main objective was to study inter-annual variation in clutch size. because we found a high rate of divorce or mate change during the period between capture and incubation (Mougeot et al. cases of mate loss to predation or failures in transmitters. Williams 1996).Fabián Casas Arenas Tesis Doctoral we still had problems to estimate the real number of eggs laid per female. sites. Moreover. Hatching success Because we were interested in natural variations in nesting success. we have only considered clutch size of each individual nest. In this analysis. and taking into account that during incubation. However. we obtained complete data sets for only four tabbed pairs (Table 1). but we acknowledge that this does no accurately reflect the real laying effort of each female. Due to the differences between years in field work effort carried out on the various sites. to determine significant differences among groups. To allow comparisons. we excluded “a priori” from the analysis all the interactions with this variable. that have been presented elsewhere (chapter 2). this may be an reasonable estimate of incubation ability and parental effort. We used a Tukey post hoc test. Finally. Predation probability was fitted to GLMz models using a binomial error distribution and a logit link function. For all these limitations. 2006a. we first analysed the probability of clutch being lost to predation of the incubating birds or the whole clutch. we considered all nests (n=65) for which we knew final clutch size. sex and year as independent variables. 1b). following a backward stepwise procedure (Crawley 1993). we considered only successful nests (n=34).001).6). P = 0. P = 0.7. sex and year in a GLMz analysis.46.049). P = 0. when no males incubated at all.01 (SAS 2001). 1a).66 % of radio-tagged females (n = 50) incubated. we first checked that there was no significant effect of hunting management models. For these analyses.78.59 = 3.0 and SAS 8. P = 0. excluding clutches that were entirely lost (agricultural practices. df = 2.5 km² (see chapter 2). P = 0. following the same procedure described above.14.161).60.07. depending on year (sex: F1. P < 0. predation. sex × year interaction: F2.16. but not between sites (χ² = 2. RESULTS Proportion of females and males incubating The probability of incubating significantly differed between sexes (χ² = 28. df = 2. df = 1. 1a) or sites (χ² = 1. In contrast. df = 3.78. The proportion of females incubating did not differ significantly between years (χ² = 1. Due to the small sample size.0053. df = 3. Laying occurred earlier in 2003 than in other years (Fig.88.Capítulo 1 Second.211.003) and by the sex of the bird incubating.63 = 1. or other nest loss causes). 1a). while the proportion of males incubating the other three years was fairly similar (Fig. P = 0.59 = 5. we analysed variation in hatching success. 94.59 = 1. 41 .24). but was explained by year (F3. the proportion of males that incubated varied markedly between years (χ² = 10. P = 0. and all game states in the study area had similar natural conditions in an overall area of about 12. All the analyses were performed with the statistical package STATISTICA 6.97 % of radio-tagged males (n = 49) did so. We considered the effects of laying date. Fig. and adjusted data by GLMz with poisson error distribution and log link function. because we were more interested in annual variation. Fig. whereas only 40. Laying dates: differences between years and between nests incubated by females or males Variation in laying date was not significantly explained by site (F2.01. This effect was mainly due to year 2005. P = 0. 2 0. the year when laying was more delayed (Fig.0 2003 2004 2005 2006 2007 d) Year Figure 1. but unfortunately. black dots (●): males). 42 . but later in 2004.4 0.0 0. excluding clutch losses due to predation) according to the sex of the incubating bird (white dots (○): females.8 0. b) mean ± SE laying date (1 = 1st of March). In the four tabbed pairs of our sample (Table 1). c) mean ± SE clutch size (number of eggs) and d) mean ± SE hatching success (proportion of eggs hatched.6 0. Incubated by females Incubated by males 100 Proportion incubating 80 60 40 20 0 80 6 a) 70 6 16 8 13 10 Laying date b) 60 50 40 30 7 16 c) Clutch size Hatching success 14 12 10 8 1. Inter-annual variations in: a) proportion (%) of birds incubating. no data are available for any tabbed pair on the year 2003. when we detected that females began incubation much after than males. males always started incubation later than females (Green 1984).Fabián Casas Arenas Tesis Doctoral Clutches incubated by males were laid earlier than those incubated by females in this year of early laying. 1b). Between-sexes differences in clutch size were significant in 2003 (F1.26. Clutch size also decreased with increasing laying date. P = 0.001. Average clutch sizes were largest in 2003 and 2007.14. df = 2. and smallest in 2005 (Fig.004).669).59 = 8. P = 0.547. P = 0.69 and 10.056). Fig.40. all years combined). Fig. P = 0. but not significant in 2004 (F1. laying date: F1.59 = 0. but varied among years (F3.10 = 0. marginally significant in 2007 (F1. P = 0. 1c). Clutches incubated by males were larger than those incubated by females (12.485.70.47.005). The probability of a clutch being lost to predators did not differ between sites (χ² = 0. 43 .21 = 4.39. 1c). P = 0.08. Incubated by females Incubated by males 25 20 Clutch size 15 10 5 0 0 20 40 60 80 100 Laying date Figure 2. sex × laying date interaction: F1. 2).59 = 4. P = 0. P = 0. black dots (●): nests incubated by males). and between sexes (F1.676) or years (χ² = 3.21 = 6. Relationship between laying date and clutch size (white dots (○): nests incubated by females. similarly so in both sexes (model controlling for year and sex. Hatching success Clutch losses due to predation.59 = 0.Capítulo 1 Clutch size Clutch sizes did not differ significantly between sites (F2.022).29.06 ± 0.59 = 54.78.66 ± 0. respectively. P < 0.49.99. df = 3.58. hatching success differed between years (χ² = 21. for nests incubated by males. df = 3.28. df = 1. the interaction year × sex being not significant (χ² = 1. but was explained by year (χ² = 9. P = 0.8 0. df = 2.26. df = 2. 3) and with clutch size (χ² = 9.32. Fig. lay date × year interaction: χ² = 2. 1d) and decreased with increasing laying date (χ² = 26.516). Fig. df = 1. P < 0.24.48. P = 0.Fabián Casas Arenas Tesis Doctoral df = 3.001.73. For nests incubated by females.6% of nests incubated by males (n = 18). Fig.957.6 0. 1d).002). df = 1.320). but only in 5.2 1. P = 0.2 0.48. 3) or with clutch size (χ² = 0.045). P = 0. df = 2. Fig. Incubated by females Incubated by males 1. Hatching success was lowest in 2007 and was lower for nests incubated by males (Fig. Variation in hatching success was not explained by site (χ² = 2. P = 0.005).0% of nests incubated by females (n = 30). df = 1. the interaction year × laying 44 .526.001. P = 0.4 0. Unhatched eggs. P = 0.0 10 20 30 40 50 60 70 80 Laying date Figure 3.757). Total losses due to predation occurred in 40. black dots (●): males).00. df = 1.923.99. df = 3.0 Hatching success 0. In contrast. P = 0. P = 0. but differed between sexes (χ² = 7.026) and sex (χ² = 3. P = 0. hatching success did not differ significantly between years (χ² = 0. We further analysed hatching success variation using clutches that reached hatching stage. excluding clutch losses due to predation) and laying date according to the sex of the incubating bird (white dots (○): females. 1d) and did not vary with laying date (lay date: χ² = 0. Relationship between hatching success (proportion of eggs hatched. P = 0.353). df = 1.23.10. P = 0. Furthermore. was poor. Servicio Integral de Asesoramiento al Regante http://crea. from none in one year. a result that stresses the importance of male contribution to partridge reproductive success.Capítulo 1 date being not significant (χ² = 3. 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. 3). humidity (% water saturation) calculated as average for each period. and rainfall (l/m2) calculated as the accumulation for each period.41 Humidity 79.27 82.46 72. Table 2.24 54.55 68. in the original distribution area of the species. df = 2. while the proportion of males incubating was highly variable among years. Weather conditions during the study period.99 13.4 78.22 5.31 11. laying occurred very late and we found the smallest clutch sizes.05. 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 .01 72. We found that almost all females surviving until late breeding season incubated a clutch independently of yearly conditions.71 3. Winter (22nd December to 21st March) and spring (22nd March to 21st to June).9 83.4 50 98 66.8 158. Clutches that were larger. P = 0. 50 % in the other three study years.98 Rainfall 149.98 10.217). including cereal.6 203. (Data take out from agrometeorological station of Ciudad Real of the SIAR.uclm.2 116.93 64.8 No males were found incubating clutches in 2005. instead of using the number of nests located (see Green 1984). in which vegetation growth. In that year.php). laid late and incubated by males had a lower hatching success (Fig.48 13. 2002-2003 2003 2003-2004 2004 2004-2005 2005 2006-2007 2007 winter spring winter spring winter spring winter spring Temperature 5. to c. a year of marked drought in our study area (Table 2). 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. nests incubated by males had larger clutches and lower losses due to predation or farming activities (chapter 2) than those incubated by females.es/~siar/webphp/resu_hist. Temperature (ºC) calculated as average for each period.42 5. under good breeding conditions. females start a clutch to be incubated by her mates later than her own. These different strategies could be associated to laying dates. because nests incubated by males late in the season have poor hatching success (see below). a year with a drier spring (Table 2). Green (1984) reported that males usually incubate the first clutch laid by females. and males take charge of the first clutch soon after finished. we still found a high percentage of males that did not incubate. Interestingly. This results suggest that. Thus. variations in breeding systems between species or populations of waders also seem to be related to the timing of laying (Blomqvist et al.Fabián Casas Arenas Tesis Doctoral population (Green 1984). Furthermore. 2001). we did not find significant variation among years in nest predation rates. about 50 %. on the year in which vulnerability of nests to predation should have been higher due to scarce vegetation (2005). However. while under poorer conditions females would start first their own clutch. Thus. In any case. 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. laying dates of nests incubated by males were earlier or similar than those of females. while in good years they would be more prone to leave a first clutch under the care of their mate. Climatic variation in mediterranean ecosystems could affect nest predation probability through differential vegetation growth (Díaz & Carrascal 2006. males did not incubate nests. 3). even in good breeding years. We also found a marked year-to-year variation in the laying dates of nests incubated by males or females. it could be expected that partridges would adjust their behaviour to perceived nest predation risk. we found that late nests incubated by males had poor hatching success (Fig. particularly taking into account that in other years. In contrast. In the two years with apparently the best breeding conditions (2003 and 2007). the opposite was found in 2004. which were overall very low for males’ nests. but also found cases of females incubating the first clutch (17%). 1990). In fact this proportion was surprisingly similar in the other three study years. Pescador & Peris 2007). females lay eggs early. males could also be more prone to start incubation earlier in good years. Predation has been considered to be a major force driving double brooding behaviour in partridges (Green 1984). Perhaps in years with relatively poor breeding conditions. Further research is needed to accurately determine the 46 . which is known to affect predation probabilities of partridges’ nests (Ricci et al. Alternatively. in which partridges laid relatively small clutches late in the season. and females would adjust their behaviour to their expectancies about male behaviour. little is known about spring diet of partridges in Spain (Rueda et al. 2000). Clutch Size Lucio (1990) pointed out the strong influence of climatic conditions on redlegged partridge productivity considering only chick survival rates. 1999. but without any information on clutch size or laying dates. leaving nests more exposed to predation during laying and incubation.Capítulo 1 constraints that control this behaviour. Watson et al. Late winter and spring rainfall is critical for plant growth. although differences were not significant (see also chapter 2). Clutch size also 47 . Lepage & Lloyd 2004). Female ability to produce eggs probably depends on available resources and could be subject to large interannual variations (Cattadori et al. Rueda et al. Green 1984). (1993) reported a similar trend for reduced clutch size in a dry year. 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. Vegetation cover is a key factor for nesting success in this species (Ricci 1985. Nest predation rate was slightly higher in the dry year. concentrating the breeding effort on smaller single clutches could be a more successful strategy if predation risk is increased due to low vegetation cover. that females could have experienced a physiological limitation during laying. secondly. in a year of drought. and with our methodology to detect nests. first. and. probably related to low food availability (Monaghan & Nager 1997. We found large differences in clutch size among years in the direction pointed out by Lucio (1990). 1992). environmental productivity and thus food supply (Peinado & Rivas-Martínez 1987. Rands 1987. In dry years. 1990). For example. in another study area in Central Spain. with smallest clutch sizes and no double brooding in 2005. vegetation development is reduced. However. alternative explanations to food limitation constraint cannot be ruled out. 2003. Thus. a year with marked drought in late winter and spring (Table 2). and nothing about the possibility of food shortage in natural conditions. which seems to be a female decision that might be based on its perception about future commitment of males to attend its clutch. we could be underestimating the frequency of clutches lost to predators before the onset of incubation. A main trait of Mediterranean climate is the high inter-annual variability and unpredictability of temperature and rainfall regimes (Blondel & Aronson 1999). Tortosa et al. Lucio 1990). that male incubation must be intimately tied to the physiological ability of females to lay two clutches. Ricci et al. These results suggest. 2002). Finally. Again. Clutches incubated by males usually are the first laid by females (Green 1984. this would imply a high frequency of poligyny that we have not detected. However. could influence breeding rates. This is a result contrasting with the study by Green (1984). laying more eggs in the nest that will be incubated by males. we cannot discard that other population parameters not considered in this study. 2003). Table 1). 1999). a behaviour relatively common in galliforms (Filchagov 1996. 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. Storch & Segelbacher 2005). this should be mainly a decision taken by females. Additionally. this would imply a parasitism rate higher or more regular than the one we have found (Casas et al. parasite prevalence (Millán et al. From captive-breeding studies. Clutches incubated by males were larger than those incubated by females. Hatching Success Infertility and death of embryos have been identified as the main cause of hatching failure in captive red-legged partridges. again. or age structure (Green 1984. including precocial species (Winkler & Walters 1983). this rarely seems to be a limiting factor of clutch size in birds. and perhaps affected by weather. 2006a). which may be more susceptible to nest parasitism due to longer exposure time. who did not find such sex-related differences in clutch size. and this was consistently observed across years. such as population density (Mougeot et al. and confirmed in some nests of red-legged partridge by genetic analyses (Casas et al. a strategy that could increase overall pair fitness. Another explanation could be that two females could be laying eggs on the same nest. 2006b). as reported in other galliforms (Cattadori et al. given the low predation rate of clutches incubated by males. Cabezas-Díaz et al. 2005).Fabián Casas Arenas Tesis Doctoral declined along breeding season. Skutch 1982). accounting for a failure rate that may be as high as 38 % of eggs (Cabezas-Díaz & Virgós 2007). 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 . particularly in galliforms (Lack 1947. However. females could be assigning more eggs to the clutch with higher survival prospects. a general rule in birds (Martin 1987). although. a trait that could also be mediated by food abundance or by a high predation risk. and confirmed in our tabbed pairs. Although body size is usually not considered a limiting factor of clutch size in galliforms. 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 suppose an additional constraint on the female’s decision to leave a clutch under the care of his mate. about 90 % (Koenig 1982). birds could not adequately warm all eggs. Lower hatching success in male’s nests may be explained by incubation capacity (Fernández & Reboreda 2007). However. 2006a). This would be consistent with the negative relationship between clutch size and hatching success. high temperatures. 49 . respectively). again parasitic eggs should be found at higher frequencies. Hatching success in nests of females can be considered within the natural values for birds. hatching failure in nests incubated by males was abnormally high. and low humidity increase the probability of failure (Cancho 1992). This might be a male’s strategy to increase their paternity in second clutches. a good deal of the investment devoted to eggs cared by males could be lost. An alternative explanation may be that parasitic eggs appear more frequently in nests cared by males (Casas et al. and these eggs would have lower hatchability. particularly late in the season (20-90 % of eggs unhatched). this could explain the negative relationship between clutch size and hatching success.Capítulo 1 humidity): long exposure periods before incubation. Clutches incubated by male partridges had poorer hatching success. There could be a limit to clutch size imposed by brood patch size. However. Arnold 1999). given that larger clutches imply longer periods of exposure. as reported by Green (1984). that would be particularly astringent on years with delayed laying: if laying starts late. Green (1984) found a similar pattern in what he defined “delayed” and “undelayed” nests (mostly male and female nests. Late in the season temperatures are higher and humidity lower. Males do not start incubating until females finish their second clutch. because above a given threshold. and have a really low hatching success to explain the large sex-related differences in hatching success we have found. thus increasing the probability of hatching failure as breeding season advances. as suggested by several experimental studies with artificially enlarged clutches (Monaghan & Nager 1997. Finally. but different population densities. female-only-parental care would be favoured. but depending on the environmental conditions. which might be much more influenced by inter-annual variations in weather conditions and food availability. females lay eggs early or late in 50 . male care would also be favoured. as well as cases of poligyny. may a be a critical work to advance within this line of knowledge. in fact. and associated re-mating opportunities. according to breeding conditions. Management Implications Although our partridge populations were subject to different game management models. 1999) suggest that population density. Charadrius alexandrinus.Fabián Casas Arenas Tesis Doctoral Implications for the evolution of uni-parental care in birds Phylogenetic analyses (Owens 2002). but often around the threshold of density proposed by Owens (2002) as the limit between species exhibiting male. a common one in galliforms (Owens 2002). male-only parental care would appear. We have also found a high rate of divorce and re-mating within the same breeding season. is the critical factor behind the appearance of female or male uni-parental care. This lack of effect of game management could to be due to several reasons. we failed to found differences in all the breeding patterns explored between game estates (see also chapter 2). Red-legged partridges could be in a situation near the female-only stage of parental care. perhaps because typical population densities of the species are often around the threshold suggested by phylogenetic analysis. The simplest explanation is the lack of effect of hunting management models on the breeding ecology of partridges. When the opposite is true. When the benefits of deserting a clutch are higher for females than for males. Male care appears only under good breeding conditions. and experimental work with key species (Kentish plover. Székely et al. This system could be considered an intermediate stage in the evolution of breeding systems. EPPs. Further research on this species. while in poor years female-only care emerges. 2007). Red-legged partridge populations may have a large variation in population density (Vargas et al.or female-only parental care (1 nest every 10 Ha). particularly comparing the occurrence and success of male brooding under similar environmental conditions. and intraspecific parasitism. Our results suggest that. due to poor re-mating opportunities under conditions of low population density. FM was supported by a NERC advanced fellowship. K. a Grant from the Ministerio de Educación y Ciencia. Ricci 1985. Spain (PAI06-0112). Ricci et al. although it can help increasing densities of young birds (Draycott et al. (1999) What limits clutch size in waders? Journal of avian biology 30 (2). & Anderson. 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.P. 51 . 2005). During this study F. D. If food availability is a limiting factor. but further research is needed to explore the effects of food supplementation on breeding ecology. (1992) Data-base Selection of an Appropriate Biological Model: The Key to Modern Data Analysis. this management tool does not always increase clutch size or improve nesting success (Hoodless et al. Barrett RH (eds) Wildlife 2001: Populations. In the studied game estates. Lorenzo Sobrino. 1999). REFERENCES Arnold. 216-220. Casas received support from a pre-doctoral grant of the Junta de Comunidades de Castilla La Mancha (JCCM). Spain (CGL 2006-11823) and from the JCCM. 1990). little is known about its effects on breeding performance. ACKNOWLEDGEMENTS We are very thankful to all game managers and hunting societies´ presidents who kindly allowed us to work on their game estates.R. Rands 1987.Capítulo 1 the season. Burnham. In other small game birds. it could be beneficial. although. Ambrosio Donate provided invaluable data and multiple help. and CYCIT projects MCYT-REN200307851/GLO and CGL2004-02568/BOS. New York pp 16-30. 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). there was not food supply that could contribute to an improved body condition during breeding season (Draycott et al. Elsevier. T. especially to Inocencio Bastante. Delfín Martín de Lucía and Jose Juan Bermejo. 2002). For red-legged partridge. In: McCullough DR. additional food supply is a common management tool.W. & Simmons. F. Cordero.J. Moreno.Fabián Casas Arenas Tesis Doctoral Blanco-Aguiar. (2006) Prevalence of different modes of parental care in birds.M.A. Biological Journal of the Linnean Society 74. (1980) The Birds of the Western Palearctic. Ardea 95.. Tenerife (España). M. 549–555. 212-213. scale and temporal dynamics of rock partridge (Alectoris graeca saxatilis) populations in the Dolomites. 52 . Proceedings of the Royal Society of London Series B 273. Cattadori. & Viñuela. Cabezas-Díaz. M. UK. E.T. (2005) Reproductive performance changes with age and laying experience in the Red-legged Partridge Alectoris rufa. A. Spain. Virgós. Morrish. Blackwell. (2006a) Parasitismo de nidada intraespecífico en la perdiz roja (Alectoris rufa). S. 540-549. Hudson. Cockburn. Casas. J. Vol. J.C. J. Equipo y técnicas de manejo. XI Congreso Nacional y VIII Iberoamericano de Etología. Journal of animal ecology 68. (2006b) Paternidad extra-pareja en perdiz roja (Alectoris rufa).. Tenerife (España). & Virgos. (2001) Successive clutches and parental roles in waders: the importance of timing in multiple clutch systems. (2003) Extra-pair paternity in the facultatively polygynous spotless starling Sturnus unicolor.. P. & Parkin. Blomqvist. XI Congreso Nacional y VIII Iberoamericano de Etología. I. (1992) Incubación. Behavioural Ecology and Sociobiology 54.J. & Viñuela. Control.J.. D. (1999) Synchrony. & Aronson. D. Cramp. Oxford. D..W. E. Spain. Oxford University Press. Dirección General de Conservación de la Naturaleza y Sociedad Española de Ornitología. R. Madrid. Fundación La Caixa. Del Moral). 1-6. J. S. (1991) The evolution of parental care. J.H.. K. 1375–1383. Pp.. 5563. Crawley. Puerto de la Cruz. & Villafuerte. Clutton-Brock. Morrish. J. J. (1999) Biology and wildlife of the Mediterranean region. New Jersey. S. D. Merler. USA. Barcelona. Wallander. II. Oxford University Press. R. & Andersson. (2003) Perdiz Roja (Alectoris rufa). (eds. Martí & J. pp. (1993) GLIM for ecologists. & Rizzoli A. R. Cabezas-Díaz. F. Princeton University Press. T.. Atlas de las aves reproductoras de España.L. 316-323. 21-27: La perdiz roja. Oxford. S. Casas..E. London. J. E. Blondel. Cancho. Puerto de la Cruz.P. P.. Ibis 147. (2007) Adaptive and non-adaptive explanations for hatching failure in eggs of the red-legged partridge Alectoris rufa. Virgos. M. Veiga. & Villafuerte. (2002) Mass loss in incubating Eurasian dotterel: adaptation or constraint? Journal of avian biology 33. Whitfield.P.P. R. Ardeola 53. (1984) Double nesting of the red-legged partridge Alectoris rufa. J. W.D. Griffith.A. Del Hoyo. A.C.. Parish. Fernández. 215–222. & Robertson. (2006) Influence of habitat structure and nest site features on predation pressure of artificial nests in Mediterranean oak forests. A. Filchagov.C. & Reboreda. Game Conservancy Annual Review 12. R. (2002) Spring body condition of hen pheasants Phasianus colchicus in Great Britain..A. J..A. S.V. 147-156. Draycott. Owens. Koenig. Draycott. & Carrascal. Duncan. 2195-2212. M. (2005) Effects of spring supplementary feeding on population density and breeding success of released pheasants Phasianus colchicus in Britain. Barcelona. J. L. Woodburn. (ed. Carroll. Wildlife Biology 11 (3). S.Capítulo 1 Deeming.. Díaz. G. (2007) Costs of large communal clutches for male and female Greater Rheas Rhea americana. Elliott. R.B. (1999) Effects of supplementary feeding on territoriality. J. 219–224. 53 .H. & Smith.E.. D. & Reboreda. P. & Carroll. Vol. Green. 261-266. Hoodless. J..A. (1982) Ecological and social factors affecting hatchability of eggs.. D. II.C..J. M. Ibis 149.. 75–78.A. D. Environment and Evolution.C.M. Rae. Ibis 126.N. breeding success and survival of pheasants. & Sargatal. D.H. Gibier Faune Sauvage 13.. 418–428.P. Auk 120. 35-38. R.I. 177182. & Sage. Draycott. (1981) Double nesting in red-legged partridges. (2002) Extra pair paternity in birds: a review of interspecific variation and adaptive function.A.I. 69–81. Spain. New York.J. Molecular Ecology 11 (11). Ludiman. I. 332-346.B.).E. S. A. (1996) Two clutches of willow grouse in the same nest. R.P. Wildlife Biology 8 (4). & Thuman. Journal of Applied Ecology 36. (1994) Handbook of the Birds of the World.A.H.F. K. R. J.N.. Holt. K. 526-536. Oxford University Press Inc. (2003) Male parental care in greater rheas (Rhea americana) in Argentina. Auk 99.M. L. Lynx Ed. M. G.. (2002) Avian Incubation: Behaviour. Fernández. R. Green. Woodburn. Pierce. (2004) Avian clutch size in relation to rainfall seasonality and stochasticity along an aridity gradient across South Africa.Fabián Casas Arenas Tesis Doctoral Lack.. (1987) Food as a limit on breeding birds: A life-history perspective. Leckie.J. F.D. 602-612. Lack. Millán.M. 270-273. & Bennett. & Peris. Peinado.M. Tizzani. J. Martin. Mougeot. R. I. 54 . 66-71. T. (1968) Ecological adaptations for breeding in birds. a species with high paternal investment. Methuen &Co. London.E.. Lucio. (1990) Influencia de las condiciones climáticas en la productividad de la perdiz roja (Alectoris rufa).P. & Rivas-Martínez. Redpath. J. (2002) Male-only care and classical polyandry in birds: phylogeny. Martin. The Auk 115. Servicio de Publicaciones de La Universidad de Alcalá de Henares.J. (1947) The significance of clutch-size. (1998) High paternity without paternity-assurance behaviour in the purple sandpiper. 1028-1046. Owens. (1997) Variation in mating system among birds: ecological basis revealed by hierarchical comparative analysis of mate desertion. & Lloyd. Gortázar.F. Ligon. P. Ostrich 75 (4). S. UK. Monaghan. 1103–1110. (2007) Influence of roads on bird nest predation: An experimental study in the Iberian Peninsula.. (2003) The effect of aggressiveness on the population dynamics of a territorial bird. I. Journal of Helminthology 76. Proceedings of the Royal Society of London Series B 264. D. S. 225-229. J. Lepage.P.T. J.G. (1987) La Vegetación de España. Annual Review of Ecology Systems 18. P. M. (1996) Nest predation and avian life history evolution in Europe versus North America: a possible role for humans? American Naturalist 147. Ibis 89. (2002) Do helmintos increase the vulnerability of released pheasants to fox predation?. E. P. D. Landscape Urban Plan 82.. Oxford University Press. 259268. (1999) The evolution of avian breeding systems. Ardeola 37 (2). 302-352.J. P. S. C. Nature 421. & Hudson.E. 737739. & Nager. Owens. A. P. & Clobert.F.. F. UK. (1997) Why don’t birds lay more eggs? Trends in Ecology and Evolution 12. & Lifjeld. ecology and sex differences in remating opportunities. F. T. 207-218. D. Philosophical Transactions of the Royal Society of London Series B 357: 283-293. Pescador. M. Madrid. 453-487.P. & Buenestado. León. M. Skutch. 269-281. SAS.. Moodie.. F. Ricci.D. Proceedings of the Royal Society of London Series B 267.C. J. Schwagmeyer.. & Purroy. J. R.J. Gibier Faune Sauvage 44. A.A. Bulletin Mensual Office Nacional de la Chasse 184. Baragaño. J. and game management on the population ecology of partridges (Perdix perdix and Alectoris rufa). & Freckleton. García.R. Biological Conservation 40..) in French Mediterranean farmlands.. NC. J.. Fundación La Caixa. (2002) Evolutionary transitions in parental care and live bearing in vertebrates.R.. & Hardling. R. J. T. St Clair. P. 127-139. Monaghan. Sáenz de Buruaga. A. (1999) Species differences in male parental care in birds: A reexamination of correlates with paternity. (1987) Hedgerow management for the conservation of partridges Perdix perdix and Alectoris rufa.Capítulo 1 Potts. Austin. & Esteve. 2163-2170. Ricci. (1990) Effect of habitat structure and nest site selection on nest predation in red-legged partridges (Alectoris rufa L. Texas. G.N. 27-40. M. Gibier Faune Sauvage 7:231-253. & Notario. Rands. & Notario. (2001) SAS/STAT User's guide.). Schnell. 2-9. EDILESA eds. M.C.. (1992) The Evolution of Life Histories. Berger. Pp.J. N. 55 . (1985) Utilization of some natural resources by red-legged partridge (Alectoris rufa) broods in an agricultural habitat of diverse cropping and stock farming.. version 8. Reynolds. R. A. A. M. (2000) Clutch size evolution under sexual conflict enhances the stability of mating systems. J..P.D. H. Spain.W. M. Smith. Rueda. Texas University Press.J. 255-261.G.D. F.D. (2002) Males matter: the occurrence and consequences of male incubation in starlings (Sturnus vulgaris). Auk 116 (2). In: La perdiz roja.C. J. (2001) Reconocimiento de sexo y edad en especies cinegéticas. Spain. Goodwin. A..01. Lucio. J. (1980) The effects of modern agriculture. 1-82. J. Mathon. (1992) Alimentación natural de la perdiz roja (Alectoris rufa L.R. Reid. 15-38. (1993) Nidification de la perdrix rouge (Alectoris rufa) dans la région de La Mancha (Espagne). Chapman & Hall. Baragaño. Behavioural Ecology and Sociobiology 51. Cary.C. Rueda. Gestión del Hábitat. D.M. 487-503. Advance Ecology Resesearch 11.F.. G. & Ruxton.D. SAS Insitute Inc. USA. Lamey. P. Barcelona. nest predation. G.F.D. Roff.L. & Moodie. (1982) Parent birds and their young. Philosophical Transactions of the Royal Society of London Series B 357.. R. Fabián Casas Arenas Tesis Doctoral Storch, I. & Segelbacher, G. (2005) Two grouse clutches in the same nest: evidence for nest site adoption in capercaillie (Tetrao urogallus). Journal of Ornithology 146, 85-88. Székely, T., Cuthill, I. C. & Kis, J. (1999) Brood desertion in Kentish plover: sex differences in remating opportunities. Behavioural Ecology 10, 185-190. Tortosa, F. S., Perez, L. & Hillstrom, L. (2003) Effect of food abundance on laying date and clutch size in the White Stork Ciconia ciconia. Bird Study 50, 112-115. Vargas, J.M., Guerrero, J.C., Farfán, M.A., Barbosa, A.M. & Real, R. (2006) Land use and environmental factors affecting red-legged partridge (Alectoris rufa) hunting yields in southern Spain. European Journal of Wildlife Research 52 (3), 188195. Vargas, JM, Guerrero, J.C., Farfán, M.A., Barbosa, A.M. & Real, R. (2007) Geographical and environmental correlates of big and small game in Andalusia (southern Spain). Wildlife Research 34 (6), 498-506. Vavalekas, K., Thomaides, C., Papaevangellou, E. & Papageorgiou, N. (1993) Nesting biology of the Rock Partridge Alectoris graeca graeca in northern Greece. Acta Ornithologica 28 (2), 97-101. Veiga, J.P., Moreno, J., Arenas, M. & Sánchez, S. (2002) Reproductive consequences for males of paternal vs territorial strategies in the polygynous spotless starling under variable ecological and social conditions. Behaviour 139, 677-693. Watson, A., Moss, R. & Rothery, P. (2000) Weather and synchrony in 10-year population cycles of rock ptarmigan and de red grouse in Scotland. Ecology 81 (8), 2126-2136. Ward, S. (1996) Energy expenditure of female barn swallows Hirundo rustica during egg formation. Physiological Zoology 69, 930-951. Westneat, D.F., Sherman, P.W. & Morton, M.L. (1990) The ecology and evolution of extra-pair copulations in birds. Current Ornithology 7, 331-369. Winkler, D.W. & Walters, J. R. (1983) The determination of clutch size in precocial birds. Current Ornithology 1, 33-68. Williams, J. B. (1996) Energetics of avian incubation. In, Avian Energetic and Nutritional Ecology. Carey, C. (Ed.), pp. 375-416, Chapman & Hall. 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 little is known about which of the many disturbances that agricultural changes have introduced in the ecosystems are behind the red-legged partridge decline. most previous studies on red-legged partridge nesting habitat have been limited to descriptions of habitat used (Potts 1980. Blanco-Aguiar 2007.1990). Villanúa et al. or problems associated with game releases. Several reasons may explain this decline. 2002). Rands 1986. Yet. has been associated with a decrease in the availability of this landscape feature (Pain & Pienkowski 1997. However. Bota et al. Rueda et al. but the most important appears to be habitat alteration. 2006. these studies have been done on populations in the northern edge of red-legged partridge range. Blanco-Aguiar et al. particularly the changes occurred during the last decades in agrarian management models (Lucio & Purroy 1992. Blanco-Aguiar (2007) has recently concluded that agricultural intensification. Potts 1980). despite its importance as a quarry species. have modified the quality and quantity of available habitat. 2000. Predation. Moreover. 60 . are the main factors behind the deep decline in red-legged partridge hunting bags in Spain during the last decades. Blanco-Aguiar et al. such as introduction of new pathologies or genetic introgression. In press). but little is known about the relative importance of all of these factors.Fabián Casas Arenas Tesis Doctoral century. Bernabeu 2000. Nevertheless. Fuller 2000). and consequently the viability of many species (Chamberlain et al. However. the main stronghold of its worldwide populations (Aebischer & Potts 1994. as in other European countries. populations of this gamebird have suffered marked declines during the last century throughout its range (Cramps & Simmons 1980. 1990). where it has considerable socioeconomic value in rural environments as a main game prey (Lucio 1998. at least locally (Nadal 1992. Blanco-Aguiar 2007). including Spain. 2004. In northern Europe. Intensification of agriculture in Spain. 2005). and field boundaries are formed instead by strips of annual vegetation (“lindes”) in unploughed land. overhunting. Martínez et al. 2001. The red-legged partridge (Alectoris rufa) is a typical species of agrarian pseudosteppes in southwestern Europe. these landscape structures are scarce. 1993). whereas few studies have considered habitat selection (Rands 1988. along with overhunting of declining populations. 2004). Ricci et al. hedgerows and other permanent field boundaries are considered important nesting habitats for this species. Ground vegetation height and cover around the nest have been described as the main factors affecting nesting success of red-legged partridges (Rands 1988. in the Iberian Peninsula. Donald et al. Ricci et al. Vargas et al. may also be of concern. but breeding success may be more influenced by other factors. 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). and reduction in predator control permits issued (Nadal 1998) has led to an increased legal or illegal control of predators. we evaluate nest habitat selection for this territorial gamebird in its most widespread habitat ecosystem. including the maintenance and development of field boundaries. and the relative importance of 61 . In this paper. such as agricultural or game management. availability of favoured nesting habitat could affect breeding density. but available information indicates that it may be highly variable (reviewed by Yanes et al. Reitz et al. Duarte & Vargas 2002). However. Previous studies showed that nesting habitat quality was a critical factor affecting breeding success (Rands 1988. Finally. A positive correlation between breeding density and the amount of suitable nesting cover has been found in this species (Rands 1986).b. 1998). This perception. the red-legged partridge. 2005). 2003). and nesting success is thus a very important parameter affecting population dynamics in this species (Potts 1980). along with recently increased legal protection of many predators. and this is a crucial piece of information to start a solution to this conflict between game management and biodiversity conservation (Valkama et al. Thus. We also present quantitative information on the factors affecting nesting success. Additionally. Habitat management is thus considered to be the main management strategy for the maintenance of sustainable wild populations (Rands 1987a.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. the “agrarian pseudosteppes”. 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. The scientific study of the impact of predators on red-legged partridge breeding success has also received scarce attention in Spain. like other ground-nesting birds (Yanes & Suárez 1995). (2002) found a high predation rate in preferred nesting habitats. affecting negatively the populations of endangered predator species (Viñuela & Villafuerte 2003). where partridges reach their highest densities (Blanco-Aguiar et al. is usually exposed to a high nest loss rate. 1990). Ricci et al. 3º 80´ W. ploughed or abandoned farmland.Fabián Casas Arenas Tesis Doctoral predation versus other causes of failure. MATERIAL AND METHODS Study area The study area covered 125 km² and was located in Campo of Calatrava (Central Spain. 1998). red fox Vulpes vulpes and feral or domestic cats Felix catus and dogs Canis familiaris (controlled by shooting). Over the three years. within the city councils of Miguelturra and Ciudad Real. 610 m a. Predator control of the most important partridge nest predators (corvids and canids. and urban areas (mainly countryhouses) cover less than 10% of the area. B and C hunting estates in 2003.l. Predator control was the main management tool applied in the study area. including just some small areas of short scrubland and pastureland mainly limited to the rocky top of hills. and Yanes et al. B and D hunting estates in 2004. and how these relate to nesting habitat. A. and a few patches of dry annual legume crops (mainly vetch Vicia sativa) and sugar beet Beta rubra. but with different intensity.). was mainly carried out over magpies Pica pica (controlled through shooting and trapping). see Herranz 2000. Field work was developed within four game estates with marked different hunting management models (see ESM).s. according to the game estate. Other crops. vineyards. We discuss our results in terms of management strategies for this important species. and only in A and D hunting estates in 2005 (see chapter 4). This is an undulated farmland area dominated by a mosaic of crops. due to policy decisions by game estate managers about permission to work in their lands. 115 adult partridges were captured in late winter/early spring (details in 62 . Field work was carried out on A. Natural vegetation areas are very scarce. Data Collection Partridge Captures and Monitoring Fieldwork was carried out in spring and early summer from 2003 to 2005. mainly cereal (particularly barley). with interspersed patches of olive groves. 38º 80´ N. ). and some nests were also known by personal communications by farmers. scrubland. Nest Monitoring Most nests (87%) were found once incubation had begun. Finally. 10 gr. First. We used cage traps with adult alive partridges inside as a decoy. Sex was determined in the field according to morphological traits (Sáenz de Buruaga et al. unpublished data). and leguminous crops and pastureland. and the date of failure or 63 . detailed description in ESM). we located birds every 1-5 days by radio-tracking. After capture. we searched for nests in habitats according to the pattern of nesting habitat selection found on the first year.Capítulo 2 ESM). and subsequently confirmed by genetic analyses of blood samples (authors. we recorded any variation in clutch size (partial predation or additional eggs). In subsequent visits (every 2 to 5 days). 2001). date. country house gardens. In subsequent years. other nests (n=50) were found by systematically searching suitable nesting habitat. Traps were baited with wheat to additionally attract wild partridges. type of habitat. and released at the capture site. and clutch size. we recorded the final fate of the clutch (nest loss or success). Nests were found in eight different habitat types (cereal. gamekeepers and shepherds. We based this selection on preliminary interviews with gamekeepers. Nest Location The nests considered in this study were located using two methods. linde. we recorded their exact position by GPS. using AOR-AR8200 multiband receptors and three element YAGI antennas. vineyard. The first time nests were located. 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). Each bird was fitted with a necklace radio-transmitter with mortality sensor (BIOTRACK. the cause of nest loss when possible. Both nest location methods (radio-tracking and systematic searching) were used all study years (Table 3). game managers and farmers. and on nesting site selection patterns described in previous studies of this species. Second. defined as all substrates with enough vegetation cover to install a nest. fallow. desertion. Also. approaching the nests only when adults were away from the nest. and also because it correspond to the width of combine harvesters 64 . we calculated habitat availability during May. also approaching the nests only when adults were not present. Other nests were classified as “early” or “late” in relation to the mean start date of incubation during the study period (17th of May. we also calculated (for cereal fields only). bad weather. we recorded data on the distance from the nest to the nearest field boundary. between 5 and 10 m. In each case. excluding replacement clutches (n=4). number of days of tracking. once the final nest fate was known. We selected strips of 5 meters because we found the highest frequency of nests within this external strip (see results). Nest loss causes were classified into six types: farming practices. hatched or disappeared). which was determined according to clutch condition (broken. and to avoid unnecessary disturbance during incubation. The exact day when incubation started was known for 61 out of 97 nests. classification into one category or other was made taking into account location date. failure cause and state of the eggs prior to failure time. Bro et al. we excluded data from these nests for the analysis (n=7). Habitat availability was measured as the proportional area of each habitat within the study area. Whenever we had doubts about when incubation started. often with one half of the shell within the other one. For the analyses of nesting. the surface covered by the area between the edge of the field and 5 m inwards. n=61). as the period when most nests were built (see above).Fabián Casas Arenas Tesis Doctoral hatching. Using GIS. All analyses were carried out exclusively with first clutches. 2000b). between 10 and 15 m and the remainder (further than 15 m from the edge). cattle trampling and unknown (detailed definitions in ESM). Nesting habitat availability We recorded the cover of each kind of habitat in each hunting estate monthly. The “no radio-tracking nests” were monitored by observation at a distance of 1-2 m. predation. or when the estimated date was around 17th May (thus potentially falling into either category). Nesting success was considered to have taken place whenever at least one chick had hatched (recognized by small regular breaks in the egg-shells. The monitoring of “radio-tracking nests” was performed by radio-tracking incubating birds at a distance of 1-5 m. and subsequently calculated the total surface of each habitat type using a GIS. noting observations in maps where all parcels were marked. Therefore. country house gardens. early or late) in the nesting habitat used. Given the importance of cereal fields as nesting habitat (see results).Capítulo 2 (and this could thus be the width that could be applied in management programs. avoiding areas with low or no cover.. we performed a Chi-square analysis on a contingency table with the variables habitat and year. we analyzed in more detail the nests located in this cover type. If variation in field margin distance was explained by year. Due to the low sample size for some habitats.e. we also explored possible differences between sexes. 1984. Statistical Analyses Nesting habitat To investigate the possible variation in the use of different nesting habitats among the three study years. we pooled the data into four categories: cereal. nest location methods and nesting period (i. We tested for differences in field margin distance according to year and sex. considering only those for which precise data on the distance from the nest to the field boundary could be obtained (n = 44). Partridges nest in habitat with well developed vegetation. linde. Additionally. we also made a similar analysis. fallow and other (vineyards. 1984). such as delay in harvesting of certain strips). 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. using a Generalized Linear Model (GLMz) with poisson error distribution and log link function. see ESM). but dividing availability of “cereal cover” in availability of the different parts of the cereal fields (peripheral strips as described above). we excluded from the analysis groves and ploughed fields. scrubland and leguminous crops). We followed Bonferroni method to determine which habitats were positively selected or avoided (Byers et al. we conducted pairwise comparisons. 65 . using separate Chi-square analyses. Similarly. nest location method. a similar procedure was carried out for nests within cereal fields. habitat cover and year and their interactions as independent variables. and due to the low sample size for some of the nest loss causes. Although nests in cereal were more commonly located by radio tracking than by nest searching. farming practices and other (unknown. we assessed the relationship between distance to field margin and nest loss causes. Nest loss causes To explore factors associated to different causes of nest loss. with field margin distance and year as independent variables. see ESM).0. hunting management. we pooled data into three categories: predation. considering nest loss causes as the dependent variable and sex.Fabián Casas Arenas Tesis Doctoral 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. one of them incubated by the male. but with markedly different frequencies (Table 1. for nests within cereal fields. following a backward stepwise procedure (Crawley 1993). differences in habitat use in relation to nest location method were not 66 . habitat cover. We employed a GLMz with multinomial error distribution and logit link function. unsuccessful=0). chapter 1). nest period. A backward stepwise procedure (Crawley 1993) was used to select the final model. Additionally. All the analyses were performed with the statistical package STATISTICA 6. sex of the incubating bird (female red-legged partridges may lay two clutches. desertion and cattle trampling). nest location method. using a similar procedure to that described above. year and their interactions as independent variables. RESULTS Nesting habitat Red-legged partridges nested in practically all habitats with vegetation cover found in the study area. bad weather. nesting period. Secondly. Green 1984. hunting management type. 121 0. df = 3. A high percentage of the nests in cereal fields (72.41).474 0.24).1110.053 0. mostly (59.09). -.72. Table 1. df = 6.0320. The average distance to the edge of the field in nests within cereal did not vary significantly between sexes (χ² = 0.045 0.144 0-0.118 0.1 %) within the first five meters (see ESM). Field margin distance was lower in 2004 (4.384 + 0 0 Expected use (pei)¹ 0.215 0-0. See ESM for a brief description of the methodology. Pattern of selection was estimated following the method outlined by Byers et al. use no different to expected.031 0.079 0-0.002 0. use significantly less than expected. or between nesting periods (χ² = 4.079 0.Capítulo 2 statistically significant (χ² = 6. 0.038 Preference* 0 0 + 0 0 0 ¹The relative area of the habitat.3360.21).136 0. P = 0.031 0.77 0.7%) were located within 10 m from the field margin.56.022 Observed use (poi)² 0.61.031 0.056 0.41).01).031 0.) 0 to 5 5 to 10 10 to 15 >15 0.124 0.645 0. (1984). use significantly greater than expected.343 0-0.158 0.079 0-0. 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).072 0.227 0. df = 1.109 0. We did not find significant differences in the frequency of use of nesting habitats among years (χ² = 6.010 95% limits 0.69 ± 6. P = 0.591 0. Red-legged Partridge nesting habitat use between 2003 and 2005 (n=97). but varied significantly among years (χ² = 9. df = 2.04 m) than in 67 .127 0.09. based on 95 % Bonferroni confidence intervals. P < 0. ²Calculated for habitat i as poi = ni/N.261 0-0.67. df = 3. *Preference: +. between sexes (χ² = 4.227 0. P = 0.0750.045 0. df = 3. compared with average availability of each habitat type for the three years during May.4120.613 0.24.634 0. P = 0. P = 0. 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. Habitat Cereal Fallow Pastureland Linde Vineyards Country house gardens Scrubland Leguminous crops Distance to field boundary (m.0110. Fabián Casas Arenas Tesis Doctoral 2003 (17. χ² = 11. P < 0. P = 0. Percentage of red-legged partridge nests those were successful in relation to year and breeding period.001). P < 0. df = 1. χ² = 6.01).94.003. No significant differences were found between 2003 and 2005 (χ² = 0. Factors affecting nesting failure Overall rate of nest loss in the red-legged partridge in our study area was relatively high (63.91.001.76.88 m. df = 1. although differences between periods varied among years 68 . and negatively scrubland and cereal fields. P < 0.001). 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. df = 1. P < 0.34). No positive or negative selection was detected for other habitat types (Table 1). Success was higher in “early nests” than in “late nests” (all years combined).94 ± 5. the most external strip (0 to 5 m from the edge) was positively selected. Table 1).99 ± 9.92 % of 97 nests). or in 2005 (31. df = 7. 70 60 50 % Success 40 30 20 10 0 2003 2004 Year 2005 Early Nest Late Nest Figure 1.95. while the area at distance further than 15 m from the field margins was negatively selected (χ² = 87. Bonferroni analysis indicated that partridges positively selected lindes. When considering availability of cereal in relation to the distance to the field edges. df = 3.68 m. Other variables had no significant effect on nesting success (Table 2). Results of the model analysing factors affecting nesting success (dependent variable) of redlegged partridges in our study area (GLMz procedure). Finally.08. we also found significant variation in nesting success in relation to nesting habitat.013 0.00 Cereal Fallow Nest Habitat Linde Other Figure 2.43.857 0.50 % Success 0. 2 2 1 1 3 1 2 wald 0. Table 2). P = 0.920 1. Nests incubated by males had higher success probability (0.54.308 3.021 0.100 P 0.Capítulo 2 (significant Year*“Nesting Period” interaction. Nesting success (mean ± 95% confidence intervals) in relation to nesting habitat for the redlegged partridge in central Spain.70 0. nests located in lindes having the highest success.30 0. because the trend was reversed in 2004 (Fig.315 0. Source of variation Year Hunting Management Location Method Sex Nesting habitat Nesting Period Year x Nesting Period d.f.019 10.141 0. 0.20 0.10 0.77) or among years (Wald = 3.17).017 For nests in cereals fields. Table 2.011 13.40 0. 1). Table 2). 69 . whereas nests within cereal fields had the lowest (Fig.338 8. P = 0.77) than those incubated by females (0.60 0. 2003-2005.754 5. 2).0015 0. we did not find significant differences in nesting success related to distance to field margin (Wald = 0. 4135 DISCUSSION In a landscape dominated by agricultural land we found that red-legged partridge nests were mainly located in cultivated substrata.97 %). which contrasts with other studies. we did not found differences in nest lost causes in relation to field margin distance (Wald = 1. we did not find that fallows and natural vegetation were positively selected by partridges in our study area. This is in agreement with the habitat selection pattern of adult birds during breeding season (Fortuna 2002). P = 0.958 < 0. Causes of failure did not significantly vary among years (Fig. where hedgerows and natural vegetation were the main nesting habitat (Rueda et al. Fallows could potentially be an important nesting habitat. Nests incubated by females were more affected by farming practices.732 P 0. nest location methods or nesting periods (Table 3). 2). 3).645 0. and negatively cereal fields. For nests in cereal fields. Green 1984. Ricci et al. Lindes occupied only 0. 2 2 1 1 3 1 wald 0.361 1.304 0.4 % of all failed nests (Fig.15. as were nests placed in cereal fields. We found significant differences in nest loss causes related to sex of the incubating bird and nesting habitat (Table 3). 1990.0027 56. but due to agricultural intensification they are an increasingly scarcer habitat in agricultural areas (Pain & Pienkowski 1997).05 < 0. Rands 1988.578 1. Table 3.215 0. Ricci et al.Fabián Casas Arenas Tesis Doctoral Nest loss causes The main cause of nest loss was farming practices (ploughing and particularly harvesting) affecting to 56. Rands 1987a). Source of variation Year Hunting Management Location Method Sex Nesting habitat Nesting Period d. 1993.173 0. 1990).76). red-legged partridges selected positively linear landscape features for nesting. Factors affecting nest lost causes (dependent variable) of red-ledged partridges in our study area (GLMz Multinomial procedure). Both in our study and previous studies (Rands 1986.001 0. On 70 .f. hunting management models. and although they were the most preferred habitat they were not the one containing more nests. Perhaps as a consequence of their scarcity and dispersed occurrence.19 % of the area. a percentage almost three times higher than the proportion of nests lost to predation (20. Differences among years in the pattern of nesting success with respect to nesting period. we did not find significant differences in nesting success in relation to distance to field boundaries. 1999. Ricci et al. data pooled for 2003-2005. particularly harvesting. and this may be forcing partridges to use negatively selected agricultural substrata. Agricultural practices. Partridges nesting close to the edge in cereal fields may benefit from increased food abundance in field boundaries (Thomas & Marshall 1999). and lindes were the most successful nesting habitat. in this species as in other galliforms (Taylor et al. nests in cereal fields were mainly located close to the field margins. 1987. both results contradicting that predation may be a problem for nests in this habitat. Because nesting habitat influenced nesting success. clearly more important than predation. and partridges positively selected the most external strip (0 to 5 m from the edge) of the cereal fields. Final nest fate of red-legged partridge nests in the study area during the study period (n=62). 2006). further supporting the importance of field boundaries.Capítulo 2 the other hand. but they may also suffer from increased predation risk in linear habitats (Haensly et al. well vegetated lindes are also relatively scarce in our study area. Bro et al. 2004 showing higher failure rate for early nests. 1990. Percentage of nests. may be due to differences in agricultural 71 . 1990). Tirpak et al. rarely used in other areas. 2000a). However. As previously reported (Ricci et al. were the main cause of nest failure in red-legged partridge. cereal fields could be considered a suboptimal unselected habitat working as an ecological trap (Battin 2004). 50 45 40 35 30 25 20 15 10 5 0 2003 2004 Success Lost due to predation Lost due to farming practices Lost due to unknown causes 2005 Figure 3. our results showed the crucial importance of lindes as a nesting habitat. early harvesting of green cereals for livestock food was particularly frequent (pers.Fabián Casas Arenas Tesis Doctoral management among years. there were large differences among study areas in relation to the intensity of predator control. perhaps it might be considered the main factor with negative effect in red-legged partridge reproduction even at a national scale. but our results show that. since it was the nesting substrate with highest breeding success. In 2004. but no significant differences in nesting success and nest loss causes among hunting management schemes were found. Main predators of partridge nests (Herranz 2000). Thus. The relatively low importance of predation in our study can not be due to the management related with predator control. The high rate of nest loss caused by agricultural practices may be the consequence of the pattern of nest location in the study area. 2006). 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). Bro et al. 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). 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. In fact. Several studies have shown that highest red-legged partridge densities are found in areas with higher 72 . Additionally. the strong negative effect of agricultural practices we are reporting may also affect partridge populations in wider areas. and therefore. and was strongly selected as nesting site too. were common in our study area. 2000b). Besides. one of the hunting management models was characterised by nonintensive predator control (see ESM). obs. a result highlighting the importance of this factor to improve nesting success of this species. at least during the incubation period. changes in the agricultural system would be a more effective management tool than predator control.). 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). Management implications As in other studies (Rands 1987a. which are generalist predators associated to human activities and buildings. slight delays in cereal harvesting could be an important tool to improve red-legged partridge reproductive success. Indeed. intimately tied to the agricultural cycle. Personal Communication).Capítulo 2 fragmentation and hedge abundance (Rands 1986. Lucio & Purroy 1992. In the Spanish “pseudosteppes” there are the largest numbers of steppe bird species in the EU (Tucker 1991). up to now. could be very important for reproductive success of this species. such as the red-legged partridge. Arroyo et al. Peiró 1992. which follow their own personal experience. 2003). the main conclusion for partridge managers. most of which are Species of European Conservation Concern (SPECs). or Montagu´s harrier (Ferrero 1995). The difference found in nesting success between sexes could be due to differences in incubation onset (Green 1984). However. It is interesting to outline that these actions could also be favourable for other species using similar nesting habitat (cereal fields). is that the key to improve red-legged partridge productivity are actions on agricultural management. obs. This result also illustrates how small differences in hatching dates or in harvesting dates. no clear proximate reasons had been presented to explain this general pattern. Our study area is a typical example of the agricultural landscape that prevails in the distribution range of red-legged partridges. stopping or delaying harvesting in a strip of 5 m surrounding the cereal fields might be an effective partridge management action. This means that the information from this study could be used to improve partridge breeding by managing agricultural areas.). while low success in cereal fields would explain low abundance on areas with large agricultural exploitations. 2002) or the little bustard (Carole Attié. such as little bustards (pers. in order to increase the availability of preferred nesting habitats. Blanco-Aguiar et al. Again. great bustards (Morgado & Moreira 2000). the pseudosteppes contain one of the greatest proportions of regularly occurring species that are SPECs (Tucker & Heath 1994). something already practiced by some "select managers”. at least in Spain. Our results show that a species with high socio-economic value. Maintaining or increasing lindes in agricultural areas along with cereal harvesting management would have a positive 73 . 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. More specifically. The negative impact of harvesting on reproductive success has been observed in the Montagu´s harrier (Castaño 1995. also suffers from the same problem and this could give course for collaboration programs between hunters and conservationists. In that sense. Tucker & M. & Bretagnolle. (http://www.R. Delfín Martín de Lucía and Jose Juan Bermejo. Jesús Martínez-Padilla. B. Lorenzo Sobrino. Carlos and Jesús Nieto Arenas helped with field work. Antonio Linares. J.es/irec/reghab/ informes..uclm. Javier Bustamante and an anonymous referee for their helpful comments of earlier drafts of the manuscript. UK. Birdlife Internacional. Battin. & Potts. pp. PhD Thesis. 74 . 214-215. J. Cambridge.F. Fabián Casas Castellanos. (1994) Red–legged partridge. Bernabeu.L.M. We are also thankful to all game managers and hunting societies´ presidents who kindly allowed us to work on their game estates. Conservation Biology 18. & Beja. R. Ambrosio Donate provided invaluable and multiple help. 1998.T. (2002) Conservation of the Montagu's harrier (Circus pygargus) in agricultural areas. Bruselas. Arroyo. Laura Iglesias. (2000) Evaluación económica de la caza en Castilla-La Mancha. Heath). Spain. and should be considered a priority among the eco-condicionality measures of the new CAP. ACKNOWLEDGMENTS Salvador Luna. Gustau Calabuig. B. (2002) Impact of hunting management practices on biodiversity. Fidel Sanchez-Campos helped with GIS and habitat availability data. Vickery et al. Unfortunately. N. Their Conservation Status. Universidad de Castilla-La Mancha. current implementation of eco-conditionality measures of CAP in Spain have not properly incorporated management of lindes as a priority (BOE 2004). (2004) When good animals love bad habitats: Ecological traps and the conservation of animal populations. Animal Conservation 5. 1482-1491. We thank Beatriz Arroyo. REFERENCES Aebischer. G. Arroyo.htm) European Commision.J. Providing financial incentives to farmers that voluntary address these concerns could also play an important role in reproductive success. Birdlife Conservation Serie nº3.Fabián Casas Arenas Tesis Doctoral effect on partridges and elsewhere in Spanish farmland (Tella et al. Birds in Europe. 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 CGL200402568/BOS. P. (eds G. V. 2002). Raimundo Real. García. especially to Inocencio Bastante. Report WP2 to REGHAB project. 283-290. Steve Redpath. 199-218. (eds. E. Journal of Wildlife Management 48..P. Bota. Spain. Martí & J. Virgós. Vol. González & J. Madrid. Spain.C.G. II.J. Ardeola 42.. 212-213. Duckworth. 771-788. Game and Wildlife Science 17. Real Decreto 2352/2004. P. Del Moral).B. (2007) Variación espacial en la biología de la perdiz roja (Alectoris rufa): una aproximación multidisciplinar. (2000a) Nest-site selection of grey partridge (Perdix perdix) on agricultural lands in North-Central France. Bro. 1050-1053. E. Atlas de las aves reproductoras de España. (1993) GLIM for ecologists. J. Barcelona. Oxford.E. G. Libro Rojo de las Aves de España. London. Atienza). 75 . & Camprodon. Dirección General de Conservación de la Naturaleza y Sociedad Española de Ornitología. R.R. pp. Mañosa.C... R. J. Chamberlain. (eds. & Villafuerte. Blanco-Aguiar. R. 1-16. Blanco-Aguiar. R. Reitz. BOE. F. Bro. Lynx edicions & Centre Tecnològic Forestal de Catalunya. K. Oxford University Press.A. & Simmons. Castaño.H.. J. sobre la aplicación de la condicionalidad en relación con las ayudas directas en el marco de la política agrícola común 309. E. (2004). (1980) The Birds of the Western Palearctic. (1995) Efecto de la actividad de siega y causas de fracaso reproductivo en una población de aguilucho cenizo (Circus pygargus) en el SE de Ciudad Real. F. C.K... J.. Reitz. R. Journal of Applied Ecology 37. M. M. M. 167-172. S. (2000b) Nesting success of grey partridges (Perdix perdix) on agricultural lands in North-Central France: Relation to nesting cover and predator abundance. & Krausman.E. Game and Wildlife Science 17. Dirección General para la Biodiversidad-SEO/BirdLife.. Virgós.R. J.A. Blackwell.L. pp. Madroño. Fuller... (2003) Perdiz Roja (Alectoris rufa).C.. Crawley. (1984) Clarification of a Technique for analysis of Utilization-Availability data. 41690-41698. S. J. J. E. & Clobert. Spain. P. A. Universidad Complutense de Madrid. & Villafuerte. PhD Thesis. Madrid. (2005) Ecology and conservation of steppe-land birds. 182-185. C. (2004) Perdiz Roja (Alectoris rufa).A. Morales. Byers. & Shrubb. R. Bunce. & Mayot.Capítulo 2 Blanco-Aguiar. D. J. (2000) Changes in the abundance of farmland birds in relation to the timing of agricultural intensification in England and Wales. Steinhorst. Clobert.J. Cramp. Vickery).D. REGHAB project. (2000) Relationship between recent changes in lowland British agriculture and farmland bird populations: an overview. Morgado. & Villafuerte.J.V. Ecology and Conservation of Lowland Farmland Birds. M. R.J. (2001) Agricultural intensification and the collapse of Europe´s farmland bird populations. FEDENCE-EEC. R. Universidad Autónoma de Madrid. (eds. Symp. S.J. 417-430. 87-100. A. G. bases ecoetológicas para tener éxito con las repoblaciones.E. (2002) Socioeconomic and cultural aspects of gamebird hunting. Fundación La Caixa. & Moreira. Grice & J. Ardeola 47.J. (1992) Problemática de las poblaciones de perdiz roja. Crawford. (2000) Efectos de la depredación y del control de depredadores sobre la caza menor en Castilla-La Mancha.E. Spain.M. nest site selection. (2002) Los sumideros de perdiz roja a lo largo del ciclo anual. (eds.F. Quails and Francolins.J. sex-ratio and clutch size of the great bustard Otis tarda in two adjacent lekking areas. Green. & Purroy. 63-92. M. Lucio & M.. J. FEDENCA. J. (1998) Recuperación y gestión de la perdiz roja en España. on Partridges. 101-126.D. P. & Meyers. Aebisher & S. Duarte.A. J. Potts.J. A. Gibier Faune Sauvage 9. Madrid. Ferrero. Dowell) First Intern. (2002) Selección de hábitat de la perdiz roja Alectoris rufa en período reproductor en relación con las características del paisaje de un agrosistema de La Mancha (España). (eds. (1984) Double nesting of the red-legged partridge Alectoris rufa. Madrid. J. Tring. Martínez. (1995) La población ibérica de Aguilucho Cenizo Circus pygargus. Barcelona. Haensly. Gestión del Hábitat. Herranz. Aportaciones a la gestión sostenible de la caza. FEDENCA). British Ornithologists' Union. pp. M. & Vargas.J. R. 332-346. Lucio. Evans. Bruselas. F.F. R. European Commission. (1987) Relationships of habitat structure to nest success of ring-necked pheasants. F. P. A.A. Viñuela.. R. Bélgica.A. 76 . Lucio. La perdiz roja. Birkan.M. La perdiz roja. Fuller. 5-16. Sáenz de Buruaga). PhD Thesis. (2000) Seasonal population dynamics. (1992) Red-legged partridge (Alectoris rufa) habitat selection in Northwest Spain. Alytes 7. pp. N. Fortuna.Fabián Casas Arenas Tesis Doctoral Donald. Green. J. Journal of Wildlife Management 51. Spain.F. Aebischer. T. 237-246. 539-560. Nadal. 25-29. 59-66. pp. Proceedings of the Royal Society of London Series B 268. & Heath. pp. 421-428. J..R. N. A. J. (eds. Ibis 126. J. Ardeola 49. Biological Conservation 40. Baragaño.R. G.R. F. 77 . V. M... & Purroy. Ricci. Rands. Ecological Research 2. Mathon J. Spain.R.. Universidad de Alicante. (1988) The effect of nest site selection on nest predation in Grey Partridge Perdix perdix and Red-legged partridge Alectoris rufa.R. Spain.) (1994) Predación. (1990) Effect of habitat structure and nest site selection on nest predation in red-legged partridges (Alectoris rufa L.W. M. (1993) Nidification de la perdrix rouge (Alectoris rufa) dans la région de La Mancha (Espagne). 3345. 2-9. Journal of Zoology 212. (1980) The effects of modern agriculture. pp. (2001) Reconocimiento de sexo y edad en especies cinegéticas. (1987a) Hedgerow management for the conservation of partridges Perdix perdix and Alectoris rufa. (coord. London. 407-418.R. J. Potts. caza y vida silvestre. P. & Pienkowski. & Fuzeau.W. J. Game & Wildlife Science 19. Gibier Faune Sauvage 7. (1998) La Bioecología de la perdiz roja. A. UK. Le Goff. (1986) Effect of hedgerow characteristics on partridge breeding densities. 127-139.J. PhD Thesis. 479-87. Berger F. The Common Agricultural Policy and its implications for bird conservation. Nadal. (2002) Landscape selection by grey partridge (Perdix perdix) for nesting in the fields of French cereal agrosystems. Lucio. Barcelona.Capítulo 2 Nadal. Ornis Scandinavica 19. J.. 2-79. Spain.W. (eds.W. M. Rueda. Sáenz de Buruaga. AedosFundación “La Caixa”. M.. 209-20. Sáenz de Buruaga). EDILESA eds. M. E.J. 231-253. (1997) Farming and birds in Europe. & Comalrena.C. (1992) Ecología de las poblaciones de perdiz roja (Alectoris rufa) en la provincia de Alicante y su aplicación a la gestión cinegética. nest predation and game management on the population ecology of partridges (Perdix perdix and Alectoris rufa). & Notario. J. Rands. 35-40.) in french mediterranean farmlands. & Esteve J. Pain D. Madrid. Journal of Applied Ecology 23. M. Reitz.W. F. (1987b) Recruitment of grey and red-legged partridges (Perdix perdix and Alectoris rufa) in relation to population density and habitat. M. Grupo Editorial V-FEDENCA. M.F.J. Rands. Garcia A. I curso.. La Perdiz Roja. Rands. M.P. León.R. A. Bulletin Mensual Office Nacional de la Chasse 184. Academic Press. Peiró. Stauffer. Fielding. D. Guerrero. Vickery. C. Trofeo 317.... J. L. & Donazár. 171-203. P. G. (2006) Land use and environmental factors affecting red-legged partridge (Alectoris rufa) hunting yields in southern Spain. 131-144.F. The conservation of lowland dry grassland birds in Europe. Conservation biology 12.. Fridhof. J.M.P. 23-27.. & Rusch. F. M. J. Redpath.1007/s10344-007-0130-2.M & Heath. Barbosa.. 188–195. Journal of Wildlife management 63. S. N. (1999) Microhabitat selection by nesting and brood-rearing northern bobwhite in Kansas. Miller. Tirpak. Redpath.M. Acevedo. J. pp.Fabián Casas Arenas Tesis Doctoral Taylor. A.L.. Agriculture. European Journal of Wildlife Research 52. (eds. Giuliano. (2006) Ruffed grouse nest success habitat selection in the Central and Southern Applachians.J. T. Marquiss & C. Tucker. S.W... Thirgood. pp. Allen. DOI 10. Viñuela.. (1994) Birds in Europe: their conservation status.. 593-604. J. Hiraldo. A. C. Korpimäki. Casas.M. (1996) El declive de la perdiz roja en el olivar. European Journal of Wildlife Research. Tella. Carter.)... J.K. UK. S. Vargas.D. G. M. G. 686-694.. M. Bittner. Galbraith). Arroyo. Pérez-Rodríguez.J... S. Ecosystems and Environment 72. S.. Igo.M. Church.. & Marshall. & Real. Goriup. Farfán.L.M. Edwards. A.. Valkama.. Agriculture.A. Viñuela. (2003) Predators and rabbits in Spain: a key conflict for European raptor conservation.. & Fuller. & Gortázar. J. (1998) Conflicts between lesser kestrel conservation and European agricultural policy as identified by habitat use analysis.. J. Batten. 37-48.C. J. D. & Villafuerte.A. Bretagnolle.A.. Bro. 78 . The Stationary Office.M.. Beja. Vargas. E. Birdlife International.G.A. 138-144. R. S. B. Birds of prey in a changing environment. J. R.F.. Journal of Wildlife management 70. J.. & Cardo.A.. Villanúa.E.. Forero. P. (1991) The status of lowland dry grassland birds in Europe..F. E. V. (2005) Birds of prey as limiting factors of gamebird populations in Europe: a review. D.M. 41-52. Alzaga. Peterborough: Joint Nature Conservation Committee. M. J. W. K. Tucker. Ecosystem & Environment 89. M. C. Thomas.W. P. & Viñuela. & Norman.J. R.G. D. Biological Reviews 80. Thompson. J. F. Kenward. & Norton. 511-526.S. (2002) The potential value of managed cereal field margins as foraging habitats for farmland birds in the UK. (eds.B. R.H. E. (In press) Sanitary risks of red-legged partridge releases: introduction of parasites. V. London. (1999) Arthropod abundance and diversity in differently vegetated margins of arable fields. Cambridge. W. Mañosa. J. (1998) La Perdiz Roja. M. I curso. Grupo Editorial V-FEDENCA. J. Madrid.. & Suárez. de la Puente. M. M. (1995) Nest predation patterns in ground-nesting passerines on the Iberian Peninsula. 79 . Yanes. 423-428. (coord. Sáenz de Buruaga). Identidad de los depredadores e intensidad de la depredación. pp. J. Herranz. La Perdiz Roja. F. Ecography 18.Capítulo 2 Yanes. 135-147.. & Suárez F. we checked if the value of “expected use” was inside the interval (no selection). Leguminous crops: peas Pisum sativum and vetch. Unknown: when we could not clearly assign failure to any of the previous causes. DEFINITION OF THE CAUSES OF NEST LOSS Farming practices: vegetation cover was mowed or harvested. Fallow: unploughed fields with herbaceous annual vegetation that had been cultivated in previous years. Cattle trampling: if there were cattle foraging inside the nest field and the eggs were found crushed. applying the formula in Byers et al. rye and cereal mix. over the interval (positive selection) or under interval (negative selection). Weather: whenever failure occurred just after a strong storm. (1984) with a Z0. Once the so-called 95 % “bonferroni intervals” of confidence were calculated. Scrubland: Mediterranean short scrubland in small patches. Country house gardens: nests found just in the external hedge or inside country house fenced gardens. hard wheat. Lastly. Desertion: eggs were found cold.003125= 2. Linde: linear annual vegetation patches in strips of unploughed land placed between cultivated plots or between the plots and tracks. Predation: when large fragments of shell were found scattered around the nest or eggs had disappeared. 80 . after birds had disappeared for at least one day. BONFERRONI METHOD (Byers et al. wheat.734369. eggs were broken and compressed into the nest or the adult partridge had not come back to the nest after harvesting. 1984) It is based on the calculation of simultaneous confidence intervals for the true proportion of utilization for each habitat. Vineyard: traditional or modern cultivation system with guiding wires. Pastureland: natural low herbaceous vegetation. oats.Fabián Casas Arenas Tesis Doctoral ELECTRONIC SUPPLEMENTARY MATERIAL (ESM) DESCRIPTION OF HABITAT TYPES FOUND TO BE NESTING HABITAT OF RED-LEGGED PARTRIDGES Cereal: barley. Red-legged partridge nests found in the three study years.Capítulo 2 Table 1. classified by hunting state. Location Method Radiotagged birds Untagged birds Total 2003 23 15 38 2004 13 25 38 2005 11 10 21 Total 47 50 97 81 . Data in first column provided for states A and C respectively.55 birds/year/hectare) During all year Yes Yes No No Yes Yes (about 500 rabbit/year) Table 2. Hunting state Year 2003 2004 2005 Total A 7♂/3♀ 10 ♂ / 6 ♀ 5 ♂ / 11 ♀ 22 ♂ / 20 ♀ B 9 ♂ / 11♀ 7♂/8♀ 16 ♂ / 19 ♀ C 5♂/4♀ D 5♂/8♀ 7♂/9♀ 12 ♂ / 17 ♀ ♂ 21 22 12 55 Total ♀ 18 22 20 60 5♂/4♀ Table 3. hunting pressure adjusted to autumn populations (0. inside the study area. classified by location method (see methods for details). the same hunting pressure all years (1. Red-legged Partridges captured and radio-tagged during the study period.26 and 0.15 birds/year/hectare) Only during late breeding season Yes No No No No Model 2 (B) 1484 Intensive High High hunting bags. hunting pressure adjusted to autumn populations (0. year and sex.35 birds/year/hectare) During all year Yes Yes Yes Yes Yes No (about 2000 rabbit/year) Model 3 (D) 548 Extensive Low Different among years. Main traits of the hunting management models in the four game states. Hunting management traits Surface covered (Ha) Kind of Exploitation Nº of hunters Hunting bag (average study period birds/year/hectare) Predator control Artificial water points Artificial food points Refuges Releases of farm-bred partridges Hunting of rabbits Controlled rabbit hunting bags Model 1 (A and C) 3145 and 1009 Extensive High Variable among years. C ou Le gu m ho in o us cr o ya ps 82 . 70 60 Frecuency (%) 50 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). and used is referred to the total number of nests analysed (n=97). Data pooled for 2003-2005. Data pooled for 2003-2005. Availability is referred to the whole area analysed.Fabián Casas Arenas Tesis Doctoral 80 70 60 Average % 50 40 30 20 10 0 Use Availability Fa l lo w ea l d e rd s re la n bl an d Li nd ns C er Vi ne rd e Sc ru ga Pa st u us e nt ry Figure 1. excluding non-vegetated habitat. Used vs available nesting habitat for red-legged partridge in the study area. Mougeot.A.CAPÍTULO 3 Consecuencias fenotípicas y sobre la eficacia biológica de la introgresión genética en poblaciones silvestres de perdiz roja Alectoris rufa Casas. J. F. En preparación .. Dávila. F. I. & Viñuela.. Phenotypic and fitness consequences of genetic introgression in wild red-legged partridges Alectoris rufa.. J. Sánchez-Barbudo. . Body condition did not differ between hybrid and non-hybrid males. chukar). aimed at increasing the productivity of farmed birds. renewing genetic pools in areas with genetic introgression. Hybridization may also be artificially produced by crossing two allopatric species in captive breeding. and tended to be higher for hybrids than for non-hybrids. Hybrid birds had lower survival rate than non-hybrid ones and this difference was mainly due to higher predation rates on hybrid birds. whereas no differences were found in females. Thus. 5. The proportion of hybrids did not differ significantly between sexes or between years. We found introgression with A. but differed between game estates. only in males. Hybrid females. 2. Anthropogenic hybridization in captivity with chukar partridge (A.Capítulo 3 ABSTRACT 1. We used a wide range of phenotypic and fitness indicators (body size. with a high socioeconomic value in rural environments. 85 . body condition. The red-legged partridge (Alectoris rufa) is currently the most important gamebird in Spain. had significantly lower plasma carotenoid concentrations. However. controlling the introgression of allochthonous genomes is a piece of vital importance for the long-term conservation of this species. survival and mortality causes) to evaluate the consequences of genetic introgression in a wild red-legged partridge population. Overall. but hybrid females were in better body condition than non-hybrid ones. but not males. and game releases have extended the problem into the wild. physiology.7 % of wild red-legged partridges. reproductive performance. 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. and preserving areas with populations in good genetic conditions are urgently needed to preserve this species as such. Synthesis and applications. favouring levels of hybridization and introgression that can have drastic ecological implications whenever these animals are introduced into wild populations. In males. 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. the releases of farm-reared partridge have become a generalized management strategy (at least 3-4 million birds released every year). Unnatural mixing of historically isolated taxa due to human-related activities has increased in recent decades. Hybrids were smaller than non-hybrid birds. chukar genes in 28. self maintenance or allocation to eggs. Variation in hatching success was not explained by genotype. Given the declines experienced by wild partridge populations over last decades. which may limit their use of carotenoid pigments for ornamental coloration. hybrid females laid larger clutches than non-hybrid ones. Laying dates did not differ significantly between hybrid and non-hybrid females. incubation probability differed between years. our results confirm a serious risk of genetic contamination of partridge populations due to game releases of farm-bred birds. 3. 6. Hybridization is a widespread phenomenon. 4. which in natural conditions plays crucial roles in the speciation and diversification of animals. Urgent management programs aimed at stopping releases of hybrid birds. The situation may be impaired by good breeding performance of hybrid females in the wild. In many taxa. favoring levels of hybridization and introgression that can have drastic ecological implications (Olden et al. which only recently has received the necessary attention (Randi 2008). due to the introduction of new species or habitat fragmentation or modification (Rhymer & Simberloff 1996). Hybridization may cause either decreased fitness ("outbreeding depression") or increased fitness ("hybrid vigor"). 2005. especially when it occurs as a consequence of human activities. 2001). relatively heterozygous individuals are often fitter than homozygous individuals (Keller & Waller 2002). Because of its potential effects on individual fitness (Allendorf et al. In birds. natural hybridization is more common between parapatric species than between sympatric species pairs. and in natural conditions. Hybridization is a widespread phenomenon (Rhymer & Simberloff 1996. leading to hybrid vigor. However. Hybridization could thus to be a threat to natural populations. the massive releases of gamebirds for hunting purposes may be a particularly widespread and worrying factor.g. 86 . Frankham 1999). Thus. Avise 2004). Randi 2008). including overdominance (heterozygote advantage) and dominance (the masking of deleterious effects).Fabián Casas Arenas Tesis Doctoral INTRODUCTION Understanding the genetic basis of fitness in natural populations has long been a central aim in ecology and evolution. Among these human-induced cases of hybridization in the wild. Avise 2004. hybridization can also create beneficial gene interactions. 2001. hybridization is also important to conservation biology. Barton 2001). Randler 2002). Keller & Waller 2002). it plays crucial roles in the speciation and diversification of animals (Rhymer & Simberloff 1996. and/or the disruption of beneficial interactions (e. Unnatural mixing of historically isolated taxa due to human-related activities has increased in recent decades. it is important to separate the evolutionary role of natural hybridization from problems associated with increasing anthropogenic hybridization (Allendorf et al. either because species recognition mechanisms may be underdeveloped in parapatric species or because of restriction mechanisms of mate choice in contact zones (Mayr 1942. Outbreeding depression is a fitness reduction seen in hybrid individuals suffering from underdominance (heterozigosity disadvantage). between genes and the environment) or intrinsically coadapted gene complexes (Templeton 1986. Partridges with allochthonous lineages have been more commonly found in game estates where farm-reared partridge releases took place (Blanco-Aguiar 2007). 2002). 2007). which has increased exponentially since the 80´s. 2004. especially in farmland areas. Anthropogenic hybridization in captivity aims at increasing the productivity of farmed birds. and has a high socioeconomic value in rural environments (Lucio 1998. Barbanera et al. Randi & Bernard-Laurent 1998. due to widespread declines in wild populations and increasing genetic introgression with allochtonous partridges (Aebischer & Potts 1994). and game releases have extended the problem into the wild. Genetic introgression in continental Spain seems to be a general pattern of human origin.). The formation of hybrid zones can be promoted by biological or human-induced invasions. due to higher productivity in farms of chukar partridges or their hybrids with red-legged partridges (Nadal 1992). 2005). the red-legged partridge and the barbary partridge (A. especially in areas where farm-bred partridges are released for hunting purposes (Blanco-Aguiar 2007). However. this small gamebird is currently considered as a “vulnerable” species. Given the problems experienced by wild partridge populations. but no cases of hybridization have been described between these two partridges species. 2007) and are widespread in the Iberian Peninsula. In the southern French Alps and Italy. and the lack of control of the genetic quality of farm-bred partridges (Blanco-Aguiar 2007). 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. Bernabeu 2000. many game managers have been releasing large numbers of birds over the last 30 years in Spain (at least 3-4 millions every year. Hybrids between red-legged partridges and chukar partridges (A. graeca). Garrido 2002). with hybrids being viable and fertile (Bernard-Laurent 1990. red-legged partridge (Alectoris rufa) interbreed with rock partridge (A. 1999. This contributes to a profitable business of captive breeding and rearing of partridges in farms. Martínez et al. where the later was introduced at the last of the nineteen century (Lorenzo & Martí 2003). barbara) are both present on the Rock of Gibraltar. chukar) have been found in an introduced population in Italy (Baratti et al. In the Iberian Peninsula. on the Island of Majorca (Tejedor et al.Capítulo 3 Natural hybridization may occur sporadically between broadly sympatric species or be confined to particular contact areas (Avise 2004). and has made of restocking one of the main 87 . The red-legged partridge is actually the most important game bird in Spain. condition. Carotenoid pigments are used by partridges either for ornamental coloration (Pérez88 . b. this management system does not appear to help the recovery of wild partridge populations (Gortázar et al. Body size might be important in a competitive context. because depending on the relative importance of outbreeding depression or hybrid vigor. such as introduction of new pathologies. However. Because males are larger than females. size might differ between introgressed and non-introgressed red-legged partridges. but it is also known that released farm-bred partridges are able to establish in the wild and breed successfully (Duarte & Vargas 2004). introgressed partridges would extend more or less rapidly within wild populations. 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 indicators of health and condition. hunting bags of partridges in recent years have recovered to reach between 3 and 4.Fabián Casas Arenas Tesis Doctoral management tools currently used in Spain. at least locally (Nadal 1992. as well as the socio-economic importance of this gamebird. we investigate phenotypic and fitness differences between hybrid and nonhybrid wild red-legged partridges in central Spain over three years. 2000. Duarte & Vargas 2002. depending on the sexes. 2000). we looked at body mass corrected for size and plasma carotenoid levels. However. BlancoAguiar 2007) that appear to benefit more from other management techniques. 2004. Because hybrid birds might have different vulnerability to diseases or predators. may also be of concern. we looked at body size. As a result. As phenotypic indicators of fitness. Millán et al 2004. problems associated with game releases. In press). and survival rates than “pure” red-legged partridges.5 million partridges hunted per year (Garrido 2002). and between females for access to mates. Moreover. and that hybrid birds are commonly found in the wild. Albeit the widespread hybridization of red-legged partridges in Spain and its potential as serious problem for the conservation of the species. condition and plasma carotenoid levels. particularly habitat management (Rands 1987a. they might also have different health. Pérez et al. in particular in intra-sexual competition between males for access to territories and mates. this information is particularly important. Villanúa et al. It is well known that released partridges in general have low survival after release in the wild (Gortázar et al. and because chukar partridges are larger than red-legged partridges (Cramps & Simmons 1980). virtually nothing is know about the fitness of hybrid birds in natural populations. Here. chapter 2). and thus the potential impacts that releases of captive bred birds may have on these populations. ploughed or abandoned farmland. 3º 80´ W. not rarely found in Spain.). We also measured the survival and breeding performance of hybrid and non-hybrid birds. Vertebrates cannot synthesize carotenoids de novo. on a 125 km² area located in Campo of Calatrava. so diet may limit ornament expression and good foragers. The study area was mainly agricultural.g. and a few patches of dry annual legume crops (mainly vetch Vicia sativa) and sugar beet Beta rubra. including just some small areas of short scrubland and pastureland mainly limited to the rocky top of hills. 2006) or for reproduction (females allocate carotenoid to eggs) (Bortolotti et al. are expected to acquire more carotenoids (Olson & Owens 1998. Because harvesting (shooting) of red-legged partridge occurred on the study area. introgressed red-legged partridges might have higher or lower breeding success and survival rate than non-hybrids ones. Blas et al. but is also known that inbreeding depression may exist in this species (Woodard et al. dominated by a mosaic of crops (mainly cereal). and urban areas (mainly countryhouses) cover less than 10% of the area. Mougeot et al. 2003). MATERIAL AND METHODS Study area We conducted the study in central Spain. 1982). and that could be a common phenomenon in small-size. Hill & McGraw 2006). Management included mainly predator control. for self maintenance (parasite resistance and immune response. 2000). Other crops. in better condition.Capítulo 3 Rodríguez 2007).s. Ciudad Real (38º 80´ N. some management was conducted for hunting purposes. Natural vegetation areas are very scarce. Thus. Differences in condition and carotenoid levels between hybrid and pure partridges would thus be indicative of differences in foraging ability and health. and are currently considered as signals of individual quality (Pérez-Rodríguez et al. provision of 89 . In addition.l. We expected hybrid birds to survive less well that “pure” wild partridges. 610 m a. in press). Farm-reared birds are often selected to maximize breeding outputs. carotenoids act as immune-enhancers and are beneficial for health and self maintenance (Olson and Owens 1998. Birds with more parasites are expected to have lower carotenoid levels than healthier birds (e. and in particular to be more vulnerable to predation. with interspersed patches of olive groves. 2007). but must ingest them. domestic farms with poor management system. vineyards. Moller et al. the other one by the male. the day incubation began (julian date.01 mm. (5) tail length. before hunting season started. Sexing was subsequently confirmed by genetic analyses using blood samples (authors. All captured birds were individually ringed and sexed from plumage. and breeding success (number of young fledged / clutch size). chapter 1). one incubated by the female. 1 = 1st of January) and measured the following: (1) body mass. 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. (3) beak length and (4) head width.5 mm. clutch size. 10 gr.5-1 ml) using a heparinized syringe. 0 = failed to hatch). using cage traps baited with wheat and with an alive partridge inside the cages as a decoy. 2005: n = 32. and (7) wing length. All measurements were taken according to Svensson (1992) and by the same person (FC). red foxes Vulpes vulpes. with a 1000g Pesola® precision scale. We also took a blood sample from the brachial vein (0. For 90 . (2) tarsus length. Breeding performance and survival We located and monitored partridges using radio-tracking 2-4 times every week from capture until October. A total of 115 adult partridges were captured in February-May (2003: n = 39. Double-brooding occurs frequently in red-legged partridges (Green 1981. All birds were released at the site of capture and monitored by radio-tracking using AOR-AR8200 multiband receptors and three element YAGI antennas. hatching success (1= clutch successfully hatched > 1chick. (6) total body length. morphology and ornaments (Sáenz de Buruaga et al.Fabián Casas Arenas Tesis Doctoral drinking stations. see chapter 4). 2004: n = 44. and the release of captive bred birds (see chapter 2 for more information).). we recorded capture date (julian date. For each bird. unpublished data). For each female we recorded whether it laid and incubated a clutch (1 =incubation. Females often lay in two nests. with a digital calliper to the nearest 0. with a ruler to the nearest 0. 0 = no incubation). 1 = 1st of April). 1984. and fitted each bird with a 10g necklace radio-transmitter with a mortality sensor (BIOTRACK. 2001). Predator control targeted mostly magpies Pica pica (controlled through shooting and trapping). For males. n =15 males) so sample size was reduced for the analyses of breeding performance.Capítulo 3 females. rufa was detected by means of diagnostic SNPs located in the cytochrome b sequence (Blanco-Aguiar 2007). poaching (hunted out of the game period). but not laying date or clutch size. For survival analyses. Alleles sizes were determined according to GeneScan 500 LIZ Size Standard (Applied Biosystems) and GeneScan Analysis Software version 3. 1989). 91 . laying date. VIC or PET and genotyped on an ABI 3100 Automated Capillary DNA Sequencer. Forward primers were labelled with 6-FAM.7 (Applied Biosystems). The cause of natural mortality was identified for 35 birds. we excluded from our analyses losses due to agricultural practices or poaching (n = 5) or unknown cases (n = 3). including mortality due to agricultural practices (1 case) or unknown causes (3 cases). We amplified 8 nuclear microsatellite loci from each sample. and was classified as predation. We chose the 8 loci for this study from a suite of loci previously developed and screened (Dávila 2005. In prep. Total genomic DNA was isolated from whole blood using a standard proteinase K/phenol method (Sambrook et al. PCR reactions were performed in a 2720 Thermal Cycler (Applyed Biosystems).). we used data collected over three years on 89 adult redlegged partridges (51 females and 38 males). NED. and other causes. clutch size and hatching success. Introgression of the maternally inherited A. Dávila et al. because we did not know the genetics of the female which laid the clutch. chukar mtDNA into A. we tested for differences between hybrids and non-hybrids in incubation probability. chukar show different allele sizes at the 8 microsatellite loci. Birds that did not survive at least 7 days after tagging and those which transmitter failed were excluded from the analyses. until death or up to signal loss (until batteries run out). A. which were monitored until October of the capture year. Digested fragments of cytochrome b were resolved by 2 % agarose gel electrophoresis and ethidium bromide post-staining. which make them diagnostic genetic markers to assess nuclear introgression by hybridization between both species. Some individuals died before breeding (n =18 females. Genetic analyses All genetic analyses were performed after fieldwork. we tested for differences between hybrids and non-hybrids in incubation probability and hatching success. Because we were interested in natural mortality. rufa and A. 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. for more details.01 (SAS 2001) and STATISTICA 6. blood samples were kept refrigerated until centrifugation (4000 rpm. Plasma carotenoid analysis After collection. tarsus length. 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 . laying date: normal error distribution and identity link function. The supernatant was examined in a Shimadzu UV-1603 spectrophotometer at 446 nm (see. plasma carotenoid concentration. Plasma carotenoid concentration was determined by diluting 60 µl of plasma in acetone (dilution 1:10). 2006). tail length.0 for statistical analyses. We categorised a bird as “hybrid” when at least one of the genetic markers showed introgression from chukar. see Table 1). probability of hatching young.Fabián Casas Arenas Tesis Doctoral The use of diagnostic markers allowed us to categorically detect chukar introgression by a simple count of diagnostic alleles at the study loci. Finally. probability of mortality or predation: binomial error distribution and logit link function. Statistical analyses We used SAS 8. Dependent variables were checked for normality (Shapiro-Wilk test). and were fitted to models using the following error distribution: (1) body mass. hatching success (eggs hatched / clutch size). We used the Princomp procedure (SAS 2001) for the Principal Component Analyses on biometrics. as an index of body size. were stored at –20 ºC until analysis. PérezRodríguez et al. 2007). included as a covariate. head width and beak length (see Table 2). with the first principal component of a PCA analyses on total body length. plasma carotenoid concentration (µg/ml) was calculated using a standard curve for lutein (Sigma Chemicals). or as “non-hybrid” when none of the markers indicated introgression. 10 min). When analysing variation in body condition. body size (PC1. The mixture was vortexed and centrifuged at 10000 rpm for 10 minutes to precipitate the flocculent proteins. (2) clutch size: poisson error distribution and log function. the dependent variable was body mass. Plasma and cellular fraction separately. wing length. (3) probability of incubation. All tests were two-tailed.001). Genetic status (Hybrid/Non-hybrid) of all individuals captured in four game estates during the study period (2003-2005). following similar procedure that described above.34. 23. sex. but differed between game estates (χ² = 16. sex and genotype. 1989). The percentage of hybrid partridges during the study period was highest in the estate were 93 . We tested whether variation in survival was explained by year. 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). n = 55. We used radio-tracking data from capture until October (throughout the whole study period) or until death or signal loss. 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 1958.7 %). Table 1.6 % of males. site and hybridization as independent variables. n = 60) or between years (χ² = 1. P = 0.50. df = 3. We analysed the probability of mortality due to predation including year. hybridization and the interactions among these explanatory variables. Game Estate Year 2003 2004 2005 Total Distance RESULTS A 2/8 2/14 4/12 8/34 1688 B 11/9 8/7 19/16 C 4/5 4/5 835 D 0/13 2/14 2/27 9781 Total Hybrid/NonHybrid 17/22 10/34 6/26 33/82 Hybridization rate in the studied populations We found introgression in 33 of 115 birds analysed (28. P < 0. and 33. P = 0. The proportion of hybrids did not differ significantly between sexes (χ² = 1. Pollok et al.247.Capítulo 3 table. df = 1. We used a backward stepwise selection to eliminate non-significant interactions or variables from the final model. For analyses of breeding performance. df = 2. Initial models included sex.46. we considered each sex separately (see above).482). year.3 % of females. 77).42 +0.36 3. Body size differed between non-hybrid and hybrid in males (F1.79. Variation in body size (PC1) was explained by sex (F1.cumulative .08. while the occurrence of hybrid partridges was much lower in the estates where no releases were performed (19. The first Principal Component (PC1) explained 64% of variation.4 % in estate D.8% 94 .08.25 -0.05). The second Principal Component (PC1) explained a further 14% of variation with tail length having the highest positive loading.59 0.36 +0.103 = 392. with all the measurements having positive loadings.5% +0.03 +0. Princomp procedure. and 7.3 %). Table 1).43 +0. Results of a Principal Component Analysis on biometrics of wild red-legged partridges (n = 107. PC1 was indicative of overall size.103 = 4. 1a). P < 0.Fabián Casas Arenas Tesis Doctoral partridges releases occurred yearly (estate B: 54.44 +0. P = 0.53 = 0.04.001.3% 77.1 % in estate A. P < 0. 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). Principal Components First (PC1) Second (PC2) Total body length Wing length Tail length Tarsus length Head width Beak length Eigenvalue Variance explained . Hybridization × sex: F1.31 -0.4 %).68 -0.50 = 4.001.5% 63.86 14.04. but not in the case of females (F1. and was used as an index of body size in subsequent analyses. followed by the nearest study area. P < 0. Non-hybrid males were larger than hybrid ones (Fig.81 63. Fig 1a) and was also significantly explained by the interaction between sex and hybridization (hybridization: F1.05).103 = 392. P < 0. where we had evidence of presence of released birds (estate C: 44. Table 2.42 +0.proportion +0. SAS 2001). males were larger than females.12 -0. 029 ± 0.73) and 2005 (19.45.013 ± 0.46 = 3.46 = 5.042).025 ± 0. variation in plasma carotenoids was significantly explained by year (F2.069) or 2005 (-0. P < 0. variation in plasma carotenoids was significantly explained by hybridization (F1. 1b). 1c).55 = 5. P < 0.43 = 0.67) than in 2003 (8. P < 0. we analysed variation in plasma carotenoid concentration by sex.49 = 0. but not by the interaction hybridization × year (F2.51 = 8. In females. After controlling for year and sampling date.108 = 7. After controlling for PC1 and year. Fig.54 = 4.46 = 13.73.50 = 4. In males.32. Differences in plasma carotenoid concentration between hybrid and non-hybrid partridges Males had higher plasma carotenoid concentration than females (F1.59.05).072 ± 0.05).05.055).33.05.52 = 1. 95 .71). variation in male body mass was not significantly explained by hybridization (F1.005 ± 0.001). P < 0. P = 0.93).57 ± 4. we analysed variation in body condition (body mass corrected for size) by sex. P = 0. In females. variation in female body mass was significantly explained by hybridization (F1. P = 0.01.43 = 0. Fig.43. quadratic: F1.55 = 6.46 = 3. After controlling for PC1.75. P < 0.47.015 ± 0. Hybrid females were heavier relative to their size (better condition) than non-hybrid females (Fig.34. 1b). Females were in better condition in 2003 (0.92. P < 0. Male condition increased non linearly with date and was higher in 2003 (0. Carotenoid concentration was higher in 2004 (17.052) than in 2004 (-0. 1c).01) and sampling date (linear: F1.94.32.Capítulo 3 Differences in body condition between hybrid and non-hybrid partridges Given the sexual dimorphism in size.98. variation in body mass was significantly explained by body size (PC1: F1. Because of expected differences between sexes in carotenoid use prior to breeding. P = 0.08.001).54 = 0.69. but not by sampling date (linear: F1.58 ± 6. P = 0.21). but not by the interaction hybridization × year (F2.07. P < 0. Hybrid females had significantly lower plasma carotenoid concentrations than nonhybrid females (Fig.50 = 1. quadratic term: F1. year and sampling date.03 ± 6.27).05) and by sampling date (linear term: F1. P < 0.005) and by year (F2.048) or 2005 (-0. P < 0. by year (F2. variation in body mass was significantly explained by body size (PC1: F1. nor by the interaction hybridization × year (F1.51 = 15.32. P < 0.05). P < 0.62.74).77).051) than in 2004 (0. P = 0. 12.73. 1c). Fig. P = 0.49 = 0. P = 0.41.00 -0.24.49 = 0.04. and c) plasma carotenoid concentration (in mg.02 0. P = 0. by sex).77).49 = 1.26.85) or hybridization (F1.49 = 0. Differences between sexes and between hybrid (black bars) and non-hybrid (white bars) redlegged partridges in: a) body size (mean ± SE score of the first Principal Component of a PCA on six body measurements. quadratic: F1. b) body condition (mean ± SE body mass corrected for body size. see Table 1).ml-1). variation in plasma carotenoids was not significantly explained by year (F2.04 19 13 b) Condition 0. P = 0. 96 . Sample size below / above error bars refers to number of birds.Fabián Casas Arenas Tesis Doctoral In males. sampling date (linear: F1.02 39 36 -0. Non Hybrid Hybrid Females 3 Males 39 13 a 2 1 Size a) 0 -1 -2 36 -3 19 b 0.04 c 25 13 41 39 Plasma carotenoid concentration 20 c) 15 20 10 5 0 Figure 1. 82. Nesting success in males was higher than in females (see to similar results chapter 2).78 ± 0.2 Non Hybrid (n = 63) Hybrid (n = 26) 0. but was explained by sex (χ² = 6.4 0.9. P = 0. Laying dates did not differ significantly between hybrid and non-hybrid females (F1.33 % ± 9.25.44 vs 33. n = 9) than non-hybrid females (9. and tended to be higher for hybrids than for non-hybrids (71.48. χ² = 3. F1. P = 0.8.30 = 6.30 = 0.35). 1.30 = 2.55.17).009). incubation probability did not differ between hybrid and non-hybrid red-legged partridges (χ² = 0. In males.2.062). the probability of hatching young did not differ significantly between hybrid and non-hybrid birds (χ² = 0.51. n = 21.96.83. df=1.72. P = 0. year × hybridization interaction: F1.24 ± 0.33.42 % ± 18. Similarly.44.15).Capítulo 3 Differences in breeding performance between hybrid and non-hybrid partridges In females. df = 1.8 Survival 0.57). P = 0.6 0.0 1 2 3 4 5 6 7 8 9 10 11 Month Figure 2.48. df = 1. df = 2. P = 0. with no significant differences between years (year effect: F2.30 = 1. P = 0. df=1. P = 0.36). Sample size refers to number of birds.01).35) or by the interaction genotype × sex (χ² = 1. P = 0. 97 . P = 0. df = 1. Mean (± SE) monthly survival probability of hybrid and non-hybrid red-legged partridges (data from all years and sexes combined). incubation probability differed between years (χ² = 9. P = 0. Variation in hatching success was not explained by genotype (χ² = 0.81. However. df=2.0 0. P = 0.013). hybrid females laid larger clutches (11. 3). while non-hybrid birds (n = 14) were predated by carnivores (50 %). df = 1. df = 4. raptors (28. Survival rate was higher for non-hybrid than hybrid birds. but were equally likely to die from other causes. depending on site (site × hybridization interaction: Wald= 7.3 % of hybrids birds (n = 26). but with different gradients across sites (Fig. 2). P = 0. Predators were mainly carnivores (red foxes.37.62.64. P = 0.00075. tended to differ between years (χ² = 5.052). P = 0.00023).46.0068) and between hybrid and non-hybrid birds. sex: χ² = 3. P = 0. feral cats and feral dogs) and raptors.63. among game estates (χ² = 19.0.Fabián Casas Arenas Tesis Doctoral Differences in survival between hybrid and non-hybrid partridges Survival rate (February to October) differed significantly between hybrid and non-hybrid birds (Z = 3. df = 1. 98 .99. df = 2.057. Differences in mortality causes between hybrid (black bars) and non-hybrid (white bars) adult partridges.43 %). P = 0. P = 0. February-October.7 % of non-hybrids (n = 59). In the final regression model for censored data. P= 0. Predation occurred in 42. P= 0. Predation probability differed between sites (χ² = 9. sex × hybridization: χ² = 7. but did not differ between sexes (Z= .65).0057). depending on sex (hybridization: χ² = 6. but only in 23. Data from 2003-2005.45.0057).011. P = 0. df = 3. df = 1. Hybrids males suffered significantly higher predation rate than non-hybrids ones.92.57 %) or unknown predators (21. Non-Hybrid 250 Hybrid Mean Partridge Survival Days 200 22 21 7 11 4 4 13 2 150 100 50 0 A B Game States C D Figure 3. Fig.41. we only found differences in the survival rate between hybrid and non-hybrids adult partridges. Hybrids birds (n = 11) were only found predated by carnivores (100 %). 1994). The confirmation of hybrid reproduction into the wild highlights threats or concerns for the genetic integrity of redlegged partridge populations. Hybrid birds may successfully breed in wild populations. Some of the hybrid birds we detected may have originated from backcrosses in the wild. The occurrence of hybrids in our study populations were. than in neighbour populations where releases did not take place during the last 15 years. we found introgression in 30 % of wild red-legged partridges. Larger clutch sizes of hybrid birds had been already reported in farmed birds (Nadal 1992) and the same occurred in the wild. 2000. and hybrid females laid larger clutch sizes than nonhybrid ones. but original introgression appeared mediated by human releases. Even if few released birds survive. rufa x graeca showed a narrower cline than expected. Using categorical mitochondrial and nuclear markers. Releases usually take place in late summer-autumn. and in a nearby population occupying a similar habitat. this would suppose that hybrid females might spread their genotypes more efficiently than non-hybrid ones. given that red-legged partridges and chukar partridges do not breed in sympatry (Del Hoyo et al. Given that hybrid females had the same probability of laying a clutch than non-hybrid ones.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. which could be constrained by natural selection favouring parental species (Randi & Bernard-Laurent 1999). and natural hybridization areas do not appear to exist (Randi 1996). rufa x chukar. and farm-bred birds have a very low survival rate during the first days after release into the wild (Gortázar et al. Natural hybrid zones of A. and similar hatching success. Blanco-Aguiar 2007). we do not know how natural 99 . The occurrence of hybrid partridges was higher in a game estate where more than 2000 reared-farm partridges are released yearly. 2004). Chukar partridges are not native in Spain. 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). Pérez et al. as documented for the first time by our study. a pattern similar to that found at a larger scale (more hybrid birds in estates where restocking takes place. however. For hybrids A. 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. this size difference could limit the spread of hybrid genotypes from males. while no size difference was found according to genotype in females. with larger males being favoured in contests. and suffered higher predation rates in central Spain. We found that hybrids survived less well. When considering condition (body mass corrected for size). Chukar partridges are larger than red-legged partridges (Cramps & Simmons 1980). Thus. more than adaptation to xeric habitat present in Pianosa Island (Baratti et al. but widespread across the Iberian Peninsula (Blanco-Aguiar 2007). in summary. which are artificial and of human origin. which could limit the spread of hybrid birds into wild populations in the long term. depending on sexes. Nevertheless. like those along the border of the southern French Alps (A. In contrast. Bernard-Laurent 1984). given their recent presence in the wild. rufa x graeca. and in fitness (survival and breeding performance) between hybrid and non-hybrid red-legged partridges. there occurrence reported here was high (30%). in the absence of predators and hunting. This could be a result of artificial selection in captive bred males (see below). 2004). contrary to our results. A better condition is often associated with greater laying capacity. Body size often plays a role in intra-sexual competition. the population increased from 10 pairs to 400 pairs in 20 years (Baratti et al. the larger size of non-hybrid males may give them an advantage over hybrid males. access to mates. Non-hybrid males were larger than hybrid ones. we did not find any difference between hybrid and non-hybrid males. rufa x chukar. so hybrid birds would be expected to be larger than non-hybrids. competition for resources. the contact zones are not limited in space. natural hybrid populations of Alectoris are restricted to limited parapatric zones. in terms of competition for territories. Differences between hybrid and non-hybrid partridges in body size and condition We found differences in several phenotypic traits. The absence of predation may have contributed to this increase in this hybrid population. 2004). and. in an introduced hybrid population on Pianosa Island. which could additionally explain the larger 100 . territory size. The effects of releases and hybridization might differ depending on prevailing environmental conditions experienced by wild populations. Besides.Fabián Casas Arenas Tesis Doctoral selection might act. In the case of hybrids between A. but hybrid females were in better condition (relatively heavier) than non-hybrid ones. In addition. hybrid birds seem to be more susceptible to intestinal parasites (Blanco-Aguiar 2007). An alternative explanation could be that hybrid males that survived over winter were those able to recover a good condition. Our results are. but hybrid males were found to be in poorer condition than non-hybrid ones (BlancoAguiar 2007).Capítulo 3 clutches found in hybrid females. Hybrid females had significantly lower plasma carotenoid concentrations than non-hybrid ones and a possible explanation might be that they were more parasitized. 2006. Mougeot et al. Differences between hybrid and non-hybrid partridges in plasma carotenoid levels In birds. Carotenoid levels also decrease with increasing intestinal or blood parasite infections as demonstrated in red-legged partridges (Mougeot et al. which have been previously associated with body condition parameters (Williams 2005). carotenoids are beneficial immune function and for resisting parasites (Blount et al. and are consequently often limited (Hill & McGraw 2006). MS. 2007). 2003). 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 contrast. October to December): hybrid females were found to be in better condition than non-hybrid ones. and are allocated by females to eggs for the benefits of offspring (Blount 2004). 2007. this does not fit with the finding that hybrid 101 . carotenoid pigments are responsible for the orange-red colour of legs. at least partly. 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). Thus. lower carotenoid levels might be indicative of greater parasite infections. However. consistent with those of a previous study conducted in autumn (during the hunting season. small males could have been selected in order to reduce aggressive behaviour towards females. a serious management problem in partridge farms (Padrós 1991). Here. eye rings and beak (Blas et al. we did not find differences in body condition between hybrid and non-hybrid males in spring. in prep) and other gamebirds (e. carotenoids must be acquired through diet.g. Pérez-Rodríguez 2007). 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). In addition. Martinez-Padilla et al. Garcia et al. In red-legged partridges. Larger clutches could be associated with increased predation risk in birds (Skutch 1982). for health related function (immune function. but we have not found this to be the case in our population of partridges (chapter 1 and 2). given that parasites typically negatively impact on host condition (e.g. Breeding performance and survival of hybrid and non-hybrid partridges Our data are the first to document breeding of hybrid partridges (A. should be investigated in future studies. hatching success or nesting success were found between hybrid and non-hybrid partridges. Furthermore. MS) and for allocation to eggs. Given that hybrid females laid more eggs than non-hybrid females. Male incubation depends primarily on the ability of females to lay enough eggs for two different clutches (Green 1984. and the consequences for offspring fitness. and to compare the breeding performance of hybrids and nonhybrids in natural populations. No differences in laying date. but that variability seemed to affect in a similar way to hybrid and non-hybrid birds. Red-legged partridge breeding performance has a marked year-to-year variation (chapter 1). Hybrid females laid larger clutches than non-hybrid ones. which has important associated benefits for offspring fitness. We also found that hybrid males tended to incubate more often than non-hybrid ones. This could have important fitness consequences. Carotenoids are allocated to eggs (yolk). with hybrids being selected for greater reproduction (laying) capacity (Nadal 1992).Fabián Casas Arenas Tesis Doctoral females were in better condition than non-hybrid females. 2003). parasite resistance.g. since hybrid females would have less carotenoid available than non-hybrid ones for sexual ornamentation. it is possible that they allocated fewer carotenoids to eggs than non-hybrid females. in hybrid and non-hybrid females. or by different allocation priorities for the available carotenoids. Blount 2004). 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. This might be a consequence of artificial selection in farms. with much higher concentrations being found in eggs laid in natural populations than in captivebreeding farms (Bortolotti et al. and are less colored). chapter 102 . mediated via maternal effects (e. rufa x chukar) in the wild. Blanco-Aguiar 2007). but had less plasma carotenoids prior to laying. Differences in carotenoid allocation to eggs between hybrid and non-hybrid females. Mougeot et al. no differences in blood carotenoid levels were found between hybrid and non-hybrid males. In males. This finding is also consistent with hybrid birds being selected for greater reproduction capacity in captivity. There could also be an important risk of hybrids spreading into populations where no releases take place. Marked susceptibility to predators is well known for partridges during the first weeks after release (Gortázar et al. 2000. which could underestimate mortality due to raptors. enough hybrids seem to survive. in game estates where releases have not been performed since at least 15 years ago. although in lower frequency. in particular by carnivores. recruit and breed for these to be maintained in natural populations.Capítulo 3 1). Hybrid birds suffered additive mortality that was attributable mainly to predation. most likely because of inappropriate antipredator behaviour in captive-bred birds (McPhee 2003). whenever aggressiveness and incubation willingness would be opposite traits. Non-hybrid birds were predated mainly by raptors and carnivores. with poor or no genetic control. this could be the result of an artificial selection to reduce aggression in caged mates (Padrós 1991). Management implications We found that hybrid birds accounted for c. 2004). These results should be interpreted cautiously. This raises 103 . and our results suggest that this may be the case in the long-term too. Blanco-Aguiar (2007) also found hybrid birds in game estates that do not release birds as a management tool. 30% of breeding birds in a natural partridge population in Central Spain. The findings that hybrids may breed as well as. 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. or hybrids becoming established in the long-term after releases. Although survival rate was lower in hybrid birds. given that foxes often scavenge on dead birds. as shown by hybrid presence. Predation is typically the main cause of mortality in farm-reared released gamebirds and partridges (Leif 1994. We found that hybrid partridges survived less well than non-hybrid ones in wild populations. Putaala & Hissa 2003). This might be because despite surviving less well. Pérez et al. Górtazar et al. those hybrids that recruit might be more productive than non-hybrid birds (greater laying capacity). 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. 2000. For that reason. but recovering the original genetic structure of populations by the same method that drove them to their current status. that is. stopping releases of hybrid birds. (c) Cataloguing important areas for the conservation of genetic purity of red-legged partridges. releases with genetically pure partridges. trying to recover the original genetic pool of the species. their populations have suffered such large declines that traditional shooting became not worthwhile (Aebischer 104 . The low effectiveness of farm-bred gamebird releases as a management tool has been demonstrated in several species (Leif 1994. the release of alien species and hybrid animals is strictly forbidden. Although grey partridges are considered a quarry species. (b) Where necessary. given that hybrid birds already breed in the populations. our results suggest that the current genetic status of Spanish partridge populations could worsen in the long-term even if releases were stopped. According to Spanish Law 4/1989 for the Conservation of Natural Landscapes and Wild Fauna and Flora. and mostly in accordance with suggestions by Blanco-Aguiar (2007). with particular reference to the largest continuous areas where restocking programs have not been performed by now. Additionally. and identifying areas where management actions should be implemented to correct the genetic status of populations. Thus. Therefore. However. controlling the introgression of allochthonous genomes is a piece of vital importance to assure long-term persistence of wild “true” red-legged partridge populations. the management strategy should not be stopping releases. associated with intensive hunting to remove hybrid birds. implementation of restocking programs with “pure” red-legged partridges.Fabián Casas Arenas Tesis Doctoral concerns about the risks and scale of introgression into the “pure” wild partridge populations. Gortazar et al. 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. and promoting management plans to avoid releases in those areas (see Blanco-Aguiar 2007 for a complete recommendation list). Putaala & Hissa 2003). It could be thought that the easiest and fastest way to solve this situation could be to forbid releases. we may recommend: (a) Implementation of a serious inspection protocol of partridge farms and game estates where partridge releases are performed. but our results are clear evidence of the poor implementation of that law. 2000. 2007). Our results definitely confirm the concerns about genetic problems that raised the status of “vulnerable” for this species (Aebischer & Potts 1994). (ed. Interespecific parasitic transmission also is a problem for biodiversity conservation (Tompkins et al. (1994) Red–legged partridge. Aebischer. Lorenzo Sobrino.R.F. pp. Gustau Calabuig. Chapman & Hall.K. Villanúa et al. Spain (PAI06-0112).C. Casas was supported by a predoctoral grant of the Junta de Comunidades de Castilla la Mancha (JCCM). N. F. In: Conservation and the Use of Wildlife Resources.. Spain (CGL 2006-11823) and from the JCCM. & Potts. Gamebird releases affect not only the species released. In press). pp. Antonio Linares.Capítulo 3 1997). and CYCIT projects MCYT-REN200307851/GLO and CGL200402568/BOS. F. R. Particular thanks are due to Ambrosio Donate. Sunderland. Leary. Publishers. G.F. but also others inderectly. 2007). Bolton). J.M. 613-622.. Allendorf. especially to Inocencio Bastante. 105 . FM was supported by a NERC advanced fellowship. M. Cambridge.J. because of overhunting (Keane et al. (eds G. Heath). Jesús MartínezPadilla. Avise. Laura Iglesias helped with the data collection. Spruell. which are causes for more concerns. (2001) The problems with hybrids: Setting conservation guidelines. Massachussets. 214-215. 2001. J. 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). natural history and evolution.W.J. USA. UK. 2005). a Grant from the Ministerio de Educación y Ciencia. Tucker & M. London. P. Inc. Salvador Luna. Birdlife Conservation Serie nº3. Birdlife Internacional. N. (1997) Gamebirds: management of the grey partridge in Britain. transmission of new parasites (Villanúa et al. ACKNOWLEDGEMENTS We thank all game managers and hunting societies´ presidents. Sinauer Associates. (2004) Molecular markers. REFERENCES Aebischer. Their Conservation Status. Delfín Martín de Lucía and Jose Juan Bermejo for allowing studying partridges on their hunting estates. 131–151. Trends in Ecology and Evolution 16. In: Birds in Europe. & Wenburg. Di Giuseppe. & Priet. Universidad de Castilla-La Mancha. Blanco-Aguiar.J. (2007) Variación espacial en la biología de la perdiz roja (Alectoris rufa): una aproximación multidisciplinar. G. Gibier Faune Sauvage 2. Viñuela. Negro.. (2001) The role of hybridization in evolution... Ammannati. J.R.F. Barilani. (2003) Carotenoid modulation of immune function and sexual attractiveness in zebra finches. L. Surai. & Dessi-Fulgheri. M. Spain. Blount. Tabarroni. N. A.. Biological Conservation 122.D. Archives of biochemistry and Biophysics 430 (1). Bortolotti.. Proceedings of the National Academic of Sciences of USA 103 (49). E. T. (2004) Carotenoids and life-history evolution in animals. 551568. M.Fabián Casas Arenas Tesis Doctoral Baratti. T.A. Bortolotti.. PhD Thesis.. Pérez-Rodríguez. 367-374. Ecol. N. Pérez-Garrido. Physiological and Biochemical Zoology 76. F. Bertoncini.H. F. Science 5616 (300). 106 .. Cappelli.. (2003) Carotenoids in eggs and plasma of red-legged partridges: Effects of diet and reproductive output... A.R. J. 79–96. Birkhead.. PhD Thesis. Bernard-Laurent. F. J. J. (2006) Testosterone increases bioavailability of carotenoids: Insights into the honesty of sexual signalling. Animal Genetics 36. (1990) Biologie de reproduction d’une population de perdrix rochassie`res Alectoris graeca saxatilis × Alectoris rufa rufa dans les Alpes me´ridionales. Barton. (1984) Hybridation naturelle entre perdrix bartavelle (Alectoris graeca saxatilis) et perdrix rouge (Alectoris rufa rufa) dans les Alpes-Maritimes. Bernabeu. Bernard-Laurent. Metcalfe.. J. N. Universidad Complutense de Madrid. (2000) Evaluación económica de la caza en Castilla-La Mancha.J. A. 57-69. Rev. J. Barbanera. & Marchant. graeca) and red-legged (A. 10-15. Spain. 45.B.F. Molecular ecology 10. A. J. 18633-18637. 29–35. Negro.A. Galliforms) populations by means of mitochondrial DNA and RAPD markers: a study from central Italy. Blount. J. 321-344. (2005) Analysis of the genetic Structure of red-legged partridge (Alectoris rufa. 125-127. Kark.. P. M. Bernard-Laurent. P. (2007) Hybridisation with introduced chukars (Alectoris chukar) threatens the gene pool integrity of native rock (A. & Surai. G. F. rufa) partridge populations. & Dini.R. Blas.. S. R.. Magnelli. 275-287. Mucci.L.. C. Biological Conservation 137 (1). F. C. G. P. D.. (2004) Introgression of chukar genes into a reintroduced red-legged partridge (Alectoris rufa) population in central Italy. & Randi. P. 230-241. M. & Mcgowan.E. A. K.J. C.Capítulo 3 Cramp. Garrido. (2005) Marcadores genéticos para detectar introgresión en aves del género Alectoris. (2005) Correlates of extinction risk and hunting pressure in gamebirds (Galliformes). (1994) Survival and reproduction of wild and pen-reared ring-necked pheasant hens. 216– 233. (2004) Field interbreeding of released farm-reared Redlegged partridges (Alectoris rufa) with wild ones. & Vargas. Lynx Ed. R. Madrid. & Vargas. 101-126. Keane. Villafuerte. de L. A. Hill. Gortázar.. (2002) Capturas de perdiz roja (Economía inducida por la caza de perdiz). Green. Ibis 126: 332-346. Madrid. L. R. J.E. Patent nº P200501569. Journal of Wildlife Management 58 (3). Harvard University Press.J. (1958) Nonparametric estimation from incomplete observations. J. & Meier. tomo I. II. 23-30. Zeitschrift fur Jagdwissenschaft 46.L. Elliott. Green. Oxford University Press. & McGraw. pp.K.L. (2002) Inbreeding effects in wild populations. A. S. & Martín. J. 141-147. Vol. (1984) Double nesting of the red-legged partridge Alectoris rufa. Biological Conservation 126. Vol.M.M.P. & Waller. R. Pp. II. 107 . J. En: Aportaciones a la gestión sostenible de la caza. E. & Sargatal. (1981) Double nesting in red-legged partridges. Game Wildlife and Science 21. 237-244. Journal of American Statistical Association 53. Dávila. Kaplan.E. Oxford. 457-481. Leif. (1999) Quantitative genetics in conservation biology. (2002) Los sumideros de perdiz roja a lo largo del ciclo anual. R. J.. Brooke.M. J. Spain. FEDENCE-EEC. A. FEDENCA. Game Conservancy Annual Review 12: 35-38.E. Lucio & M. Spain. J. Cambridge. (eds.L. Del Hoyo. Sáenz de Buruaga). Keller. D. A. (1994) Handbook of the Birds of the World. (2000) Success of traditional restocking of red-legged partridge for hunting purposes in areas of low density of northeast Spain Aragón..F. 55-61. M. Aportaciones a la gestión sostenible de la caza. G. Duarte. Duarte. Barcelona. Trend in Ecology and Evolution 17. (1980) The Birds of the Western Palearctic. K. & Simmons. 501-506. (2006) Bird coloration: Function and evolution. Genetical Research 74. J. Frankham. P. Evolution 4 (1).. Spain. Mougeot. Leckie. R. Møller. bases ecoetológicas para tener éxito con las repoblaciones. (2000) Carotenoid-dependent signals: indicators of foraging efficiency. Saino.D. R.. Martínez. In: La perdiz roja. & Villafuerte. J.E. (2007) Nematode parasites reduce carotenoid-based signalling in male red grouse. J.C. (1998) Recuperación y gestión de la perdiz roja en España. J. I. V. J. Sumozas. P. Functional Ecology 21... & Surai. European Commission. REGHAB project. F.C. condition.. (2003) Perdiz Moruna (Alectoris barbara). A.. Ninni. (1992) Problemática de las poblaciones de perdiz roja. FEDENCA. (2007) Parasites. McPhee. Padrós. & Terraube. Bruselas. Olson. 886-898. Mayr. Journal of Avian Biology Nadal.A. Fundación La Caixa. Mougeo. La perdiz roja. R.D. AEDOS. Pérez-Rodríguez. M. P. pp. Presente y futuro. risky or required? Trends in Ecology and Evolution 13. Barcelona. & Martí. J. L. C. Barcelona. 710.. (2003) Generations in captivity increases behavioural variance: considerations for captive breeding and reintroduction programs.. Douglas. Gortázar.J. F. 701-707. (eds. Biard.. 2036-2038. pp. Mougeot. Parasites. 1991. 214-215. 71-77. Biological Letters 3. Pérez-Rodríguez. In La perdiz roja. Journal of Wildlife Management 68.P. D. (2002) Socioeconomic and cultural aspects of gamebird hunting. Martínez-Padilla. Biological Conservation 115. J.A. N. immunocompetence or detoxification ability? Avian Poultry Sci Rev 11.M.. R. M.. & Owens.F. Redpath. Fundación la Caixa. Gestión del Hábitat. Bélgica. testosterone and honest carotenoid-based signalling of health. L.. & Bortolotti. & Douglas. Conservation biology 19.137-159. 263-288. N.F. 108 . S. (2005) The human dimensions of biotic homogenization. Blount. 87-100.. (1998) Costly sexual signals: are carotenoids rare.161–164.E.Fabián Casas Arenas Tesis Doctoral Lorenzo.R. J. F. (MS).t F. Martínez-Padilla. J. (2004) A comparison of the helminth faunas of wild and farm-reared red-legged partridges. Del Moral).P. L. Madrid: 63-92. J. Spain.. Martí & J. Madrid. Dirección General de Conservación de la Naturaleza y Sociedad Española de Ornitología. Situación actual del sector.R. (1942) Ecological factors in speciation. Millán. & Villafuerte. Lucio. J. Viñuela. G. A. 510-514. M. pp. J. Atlas de las aves reproductoras de España. cellular immunity and carotenoid-based ornamentation in male redlegged partridge Alectoris rufa. Olden. Houston. E. Pérez-Rodríguez.. C.. C. M. D.. Randler. Universidad de Castilla-La Mancha. Pérez-Rodríguez. Díez. (1998) Introgression of red-legged (Alectoris rufa) allozyme and mitochondrial DNA in rock partridge (Alectoris graeca) Alpine populations: The population genetic consequences of natural hybridization.R. Randi. 882-888. Bunck. Alonso-Alvarez... Gaudioso. D. 56-60. Pérez-Rodríguez. Rhymer. Alonso. Putaala. (2004) Use of radiotracking techniques to study a summer repopulation with red-legged partridge (Alectoris rufa) chicks.R. Molecular Phylogenetics and Evolution 6. M.W. 116. Population genetics of a hybrid zone between the red-legged partridge and rock partridge. (1987a) Hedgerow management for the conservation of partridges Perdix perdix and Alectoris rufa.. L. Carotenoid-based bill and eye ring coloration as honest signals of condition: an experimental test in the red-legged partridge (Alectoris rufa). A mitochondrial cytochrome b phylogeny of the genus Alectoris partridges. Annual Review of Ecology and Systematics 27. C. 214-227. (2008) Detecting hybridization between wild species and their domesticated relatives.. & Bernard-Laurent. Gibier Faune Sauvage 15.. 127-139. J. C. (1989) Survival analysis in telemetry studies: the staggered entry design. (2007) Repeated sampling but not sampling hour affects plasma carotenoid levels. (1996). A. testosterona y carotenoides.A. 7-15. Journal of Wildlife Management 53. (in press). 435-444. Rands. E. (1996) Extinction by hybridization and introgression. E. PhD Thesis.M. 285. Animal behaviour 63: 103-119.. S. M. Spain. C.A. A. 137-145. & Bernard-Laurent. K. (2007) Señales fiables en la perdiz roja (Alectoris rufa): condición física.E. & Curtis.H. Alonso-Alvarez. Biological Conservation 40.M. E. L.R. C.Capítulo 3 Pérez. J. Randi. A. R. Randi. & Viñuela.W. Winterstein.293. 407-418. Molecular Ecology 17. 324–337. V. J. Randi. 109 . mixed pairing and female choice. & Viñuela. P. Olmedo. (2003) Breeding dispersal and demography of wild and handreared grey partridges Perdix perdix in Finland. Wildlife Biology 4. J. Poultry Science 83.R. L. Journal of Zoology 212. Auk. E. & Bartolomé. & Hissa. (1999). Naturwissenschaften. (1987b) Recruitment of grey and red-legged partridges (Perdix perdix and Alectoris rufa) in relation to population density and habitat. Rands.D.. Pérez-Rodríguez. & Simberloff. Biochemical and Zoology 80. 83-109. Physiological. Pollock. (2002) Avian hybridization. J. D. 39-48. Texas University Press. & Arruga M. (2001) SAS / STAT User's guide. Sanitary risks of red-legged partridge releases: introduction of parasites.. Hadjisterkotis.M. Viñuela. Sambrook. Tompkins.. A. 110 . Aebischer. Second edition. USA. Svensson. Cold Spring Harbor. Ibis 149 (2). (1986) Coadaptation and outbreeding depression. 405-406. M. N. Casas. eds... Sinauer Associates..J. 1579-1584.. version 8. L. Morales. 179-182.E. A. Greenman. C.R. Sunderland. DOI 10. Villanúa. T. Tejedor. Journal of Applied Ecology 44 (5). (2001) Reconocimiento de sexo y edad en especies cinegéticas. T.A.. J. USA.V. Fritsch.. & Purroy.F..T.. the science of scarcity and diversity. pp 105-116 (Soulé. Pérez-Rodríguez. Hudson.01. Acevedo. SAS. León. G. & Maniatis. Texas. SAS Insitute Inc. E. P. J. F. Spain. L. (2007) The relative effects of raptor predation and shooting on overwinter mortality of grey partridges in the United Kingdom. E.. (1989) Molecular cloning: a laboratory manual. A negative effect of red-legged partridge Alectoris rufa releases on steppe bird conservation?. (2007) First occurence of Eucoleus contortus in a little bustard Tetrax tetrax. Austin. E.V...). (2005) Mechanisms underlying the costs of egg production. Poultry Science 61. M. M. Mautner. Parasitology 122.. (1982) Parent birds and their young... P. Cold Spring Harbor Laboratory Press. EDILESA eds. L.1007/s10344-007-0130-2. Viñuela. (1992) Identification guide to European passerines. (2001) Differential impact of shared nematode parasite on two gamebird hosts: implications for apparent competition.. 972-982. Templeton. Woodard.J. Villanúa. M. Abplanalp.. H. Monteagudo.J. Bioscience 55. Gortázar. (In press). A. & Ewald. European Journal of Wildlife Research. S. F. Williams. Skutch. 187-193. V. Potts. D..F.. L. Massachusetts.. & Gortázar. C. A. (2007) Introgression of Alectoris chukar genes into a Spanish wild Alectoris rufa population. Cary. NC. Inc. & Snyder. E. D. Svensson. M. New York. (1982) Inbreeding depression in the redlegged partridge. García de la Morena.. Watson. J. Stockholm. L. D. F.Fabián Casas Arenas Tesis Doctoral Sáenz de Buruaga. J.B. J.V. Lucio. Casas.L. In: Conservation biology.R. Journal of Heredity 98(2). Alzaga. . M.. & Viñuela. F.. en evaluación.T. 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. J. Casas. Calero-Riestra. J.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. . In particular. Møller 1997.Capítulo 4 ABSTRACT 1. other lineages followed the opposite pattern. With the application of molecular-based protocols. the genetic structure of such parasites at small spatial scale remains poorly explored. O’Brien & Evermann 1988. 2007). Indeed. Hudson et al. We found an unusually high prevalence (50 %) of Plasmodium spp. host population dynamics. the application of molecular-based protocols has widened our knowledge about parasite diversity in wild populations of hosts. behavioural sciences. 4. and substantial differences in spatial distribution of lineages among the four populations studied. Recently. because parasites and infectious diseases can largely affect life history traits of their hosts (Price 1980. anthropogenic changes on the environment. along with the high degree of host specificity (Bennett & Peirce 1988. We examined the distribution of avian malaria parasites infecting resident avian hosts (red-legged partridge Alectoris rufa) at local scale. wildlife management and conservation biology (Hamilton & Zuk 1982. While some closely-related parasite lineages achieved high occurrence in game estates without introduced farm-reared partridges. Bensch et al. Bensch et al. Assessing the consequences of human management on hosts is essential to understanding the implications of such phenomenon for wildlife conservation and disease control. 113 . Synthesis and applications. Loye & Zuk 1991. recent advances have been done in our knowledge of how avian malaria parasite prevalence and community structure vary over time and space. such as local introduction of parasites in the wild via releasing farm-reared birds could influence parasite evolution. parasitology. being more abundant in game estates with releasing activity than in sites without released birds. one lineage previously recorded in other avian hosts appeared exclusively in game estates with releasing activity. Waldenström et al.. At this study-scale. 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. Due to this remarkable genetic variation. 2. ecology. whereas the dominant lineage showed higher occurrence in non-restocking populations. However. Our results support the hypothesis that local introduction of gamebird species is an important factor affecting parasite distribution at local scale. 2004. 3. Lively & Dybdahl 2000). with particular emphasis on the effect of human activity (releasing farm-reared birds for hunting purposes) on the spatial structure of lineages. 2002. and host-parasite interactions. 2007). INTRODUCTION The interest on parasite-host relationships and their effects on wild animal populations are currently spread across many disciplines such as evolutionary biology. 2000). 1994. host population dynamics. 2004). Bensch et al. having potentially negative effects on the survival and fitness of several avian species (Atkinson & van Riper 1991. Bensch et al. For example. the genetic structure of parasites at small –local– spatial scale remains poorly explored (Fallon et al.g. although human-induced environmental changes may profoundly alter the spatial genetic structure of parasite and host populations. Pérez-Tris et al. Wood & Cosgrove 2006. In this context. 2007). Gamebirds. despite their potential in determining local prevalences. Therefore. community composition. due to differences in pathogenicity among parasite lineages and/or differences in host susceptibility (Foster et al. Villanúa et al. in press). Recent studies indicate that genetically differentiated lineages of avian malaria may display different pathological effects on the same hosts (e. 2006. 2008. and host-parasite interactions (Benkman et al. 2006. particularly red-legged partridges (Alectoris rufa). Fallon et al. important recent advances have been done in our knowledge of how prevalences and community structure of parasites vary over time and space (e. 2005). 2000). Kimura et al. Valkiūnas 1993.Fabián Casas Arenas Tesis Doctoral Bennett et al. Smith & Bernatchez 2008. dispersion patterns. 2007). the introduction by humans of parasite species into new environments can largely influence parasite evolution. Moreover. or on host resistance to parasite lineages (Westerdahl et al. 2007). Bensch et al. on the ability of parasites to disperse among hosts (Pérez-Tris & Bensch 2005). provide a particularly interesting model for this purpose. avian malaria parasites have become a powerful model for the study of ecology and evolution of parasites and their hosts (Lively & Dybdahl 2000. 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). 2005. However. parasite virulence and pathogenicity of different lineages. and red-legged 114 . Avian malaria is the most widespread and genetically diverse vector-transmitted avian disease. Merino et al. 2005). management of some wild species for hunting purposes are crucial cases in which human actions may be modifying at large scales genetic structure.g. and thus. Small-game hunting in Spain (mainly based on rabbits Oryctolagus cunniculus. and life histories of both parasites and hosts (Gortázar et al. Randi 2008). the influence of humans in host-parasite complex have been traditionally overlooked. and growing empirical evidence indicates that this kind of human-induced changes are more common than previously thought (Smith & Bernatchez 2008). as recently reviewed in a compelling monographic issue of Molecular Ecology (January 2008). unpublished data). After releasing partridges into the wild. The possibility of released partridges dispersing intestinal parasites into wild populations.Capítulo 4 partridges) generates an economical movement of more than 210 millions of euros each year in Spain. along with the scarcity of birds in the wild. We also examined the effect of human activity (releasing farm-reared birds) on the spatial distribution of avian malaria 115 . determining the spatial distribution and abundance between lineages. b. The four study areas follow contrasting game management models. Villanúa et al. in four populations of red-legged partridges. because natural populations should have lower resistance towards parasites to which they have no previous contact (Newton 1998). To our knowledge. more than 4 million farm-reared partridges are estimated to be released yearly for hunting activities in Spain (Garrido 2002). as well as transmission of new parasites to other sympatric bird species have also been reported.and inter-specific contacts between infected and uninfected individuals. Here we examine the spatial distribution of avian malaria populations infecting wild resident red-legged partridges at a local scale. optimal conditions for propagation of parasites into new environments. Such a phenomenon may indeed be of great conservation concern. Besides. Our aim was to characterize avian malaria parasites in the four populations in central Spain. Alonso et al. in press). but successful settlement and breeding in the wild of released partridges has been proved (Duarte & Vargas 2004). 2005). 2000. and thus the capacity of each malaria lineage to disperse among host populations. the increased density of individuals at local scale could increase intra. no specific pharmacological treatments for blood parasites in farm-reared partridges are used at all in Spain. 1986). The number of released bird that survive after their first “hunting season” (from august to January) is potentially low (Gortázar et al. they could also modify the evolutionary course of parasite communities. 2004a. since although local introductions of parasites may be innocuous. As a consequence of the great demand for partridges to hunt. 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. but it is expected to cause high mortality rates. and the potential effect of these parasite introductions should not be negligible (Millán et al. affect viability of wild or released partridges. or even cause local extinctions (Warner 1968. from no releases to intensive hunting of released partridges. the potential impact on hosts derived from local introduction of new parasites remain poorly studied. van Riper et al. vineyards. 610 m a. The four sampling sites had similar landscape. and D. Natural vegetation areas are very scarce.l. and moderately wet and cold winters.s. Fig. 38º 80´ N.1).8-11. and small patches of Mediterranean scrub.1 km-distant (game states A. mainly on the top of hills.). Sampling sites around Ciudad Real city. C. with interspersed patches of olive groves. Figure 1. but differed markedly in game management 116 . 3º 80´ W. The climate is Mediterranean with marked continental character. reflected in dry and hot summers. We obtained adult redlegged partridges blood samples in early spring (February and March) during 20032005 from 4 sampling sites 1. dry annual legume crops (mainly vetch Vicia sativa) and sugar beet (Beta rubra). B.Fabián Casas Arenas Tesis Doctoral lineages. discussing the implications of such phenomenon for wildlife conservation and disease control. The four host populations studied were indicated by different colours. limited to a few parcels of pastureland and fallow. Habitat is characterized by undulated farmland mainly aimed to cereal cultivation (mostly barley). MATERIALS AND METHODS Study populations and field procedure The study area comprises 125 km² located in Campo of Calatrava region (Central Spain. central Spain. Capítulo 4 systems. followed by a final amplification with the primers HaemF and HaemR2 (Bensch et al.4 mM of each primer. In game state C farm partridges were also detected in the field in lower numbers and more sporadically. A total of 115 adults were caught under license using cage traps with an alive decoy (adult red-legged partridge inside the cage). Reactions started with 3 min at 94 ºC. and 0. Avian malaria diagnosis Blood samples were obtained by ulnar venepuncture and stored in 99% ethanol until molecular analysis. In both steps. probably came from game estate B (see results chapter 3).5µl of each final reaction on 2% agarose gels stained with ethidium bromide and using 1xTAE buffer. 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). One of the game estates sampled (B) followed an intensive management model with more than 2. The samples were screened for the presence of Plasmodium and Haemoproteus using nested polymerase chain reactions (PCR) protocol (Waldeström et al. 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). 1. DNA was extracted from samples using standard NH4Ac methods. All samples with 117 .25 units of Taq DNA polymerase (Biotools). We first evaluated the quality of extracted DNA by electrophoresing 2 µl of the extract in 2% agarose stained with ethidium bromide. and baited with wheat.and post-PCR work were performed with different material and in different sections of the laboratory to avoid contamination. designed to amplify a 479-bp fragment of the mitochondrial cytochrome b gene of both parasite genus. and they were terminated by a 10-min extension at 72 ºC. The method started with a pre-amplification using primers located outside the target fragment (HaemNF and HaemNR2). Pre. followed by 20 cycles (first step) or 30 (second step) of 30 s at 94 ºC. We evaluated 2. 2000).e. Finally. and visualizing it under UV light. 0.125 mM of each nucleotide. We repeated the protocol three times to confirm negative infections.5 mM MgCl2. 0. and diluted to a working concentration of 25 ng/ml. 2004).000 farm-reared partridges released each year. 30 s at 50 ºC and 45 s at 72 ºC. The PCR tests were performed in two separate runs with positive (i. DNA from individuals with known malarial infections) and negative (ddH2O) controls. 1xPCR buffer (Biotools). we explored the clustering of our lineages. Valkiūnas et al. the cyt b sequences of most morphological species of avian Haemosporidia are clustered together into monophyletic clades (Beadell et al. Therefore. 2007). 2004). 2007. which were assigned to a given morphospecies when included into the same monophyletic clade. 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. Despite different lineages representing the same morphospecies often diverge in molecular sequence and probably may represent truly different species (Bensch et al. We used the MicroSpin s-400 HR columns (Amersham Biosciences) to purify PCR products. Then. which were sequenced from both ends using a Big Dye Terminator Kit.g. and some avian malaria cyt b lineages with less than 0. Defining parasite lineages We aligned and edited DNA sequences using Clustal W (Thompson et al.7 (Applied Biosystems). Martinsen et al. 2002). and DNA sequences were determined using an ABI 3130 automated sequencer (Applied Biosystems). Valkiūnas et al. Because many of the sequences differed by only few sites of the 479 examined. and recent works have linked morphospecies and molecular sequences (e. 2007). 1994) and Bioedit (Hall 1999).Fabián Casas Arenas Tesis Doctoral positive PCR reactions were successfully sequenced from both ends. and 6 sequences from at least 3 different Haemoproteus morphospecies). with published sequences of other avian malaria parasites registered in GenBank. The sequencing reactions were cleaned on standard Sephadex columns. discarding sequences with ambiguous sites (then amplified and sequenced again) to assess the quality of the sequences. Reading data were processed with the ABI PRISM1 Sequencing Analysis Software v3. different Plasmodium and Haemoproteus morphospecies have been genetically characterized. 2004). 2006.5% sequence divergence may represent different species (Bensch et al. Phylogenetic relationships among parasite lineages were estimated using different primate malaria 118 . Here. we used a sequence divergence of at least one nucleotide to define lineages (Waldenström et al. Although we did not have information on the morphological identity of our lineages. the same person (JTG) examined carefully each sequence at least twice. We tested for two alternative scenarios: (1) genetic structure resulting from differentiation among the four sampling game estates. 1992). We also used neighbor-joining (NJ) and maximum parsimony (MP) tree reconstruction methods to ensure consistency of the results. We performed the model of nucleotide substitution that best fitted the data (selected among 56 models tested by PAUP*). we grouped together those malaria lineages that tentatively belonged to the same species (resulted from the ML phylogenetic tree. 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.0 (Swofford 2002) to construct a maximum likelihood (ML) phylogenetic tree of all cytochrome b lineages. We used PAUP* 4. “species” (clades a. Excoffier et al. 2002). we analysed the genetic structure of our parasites pooling together lineages that resulted monophyletic with respect to morphological species in all phylogenetic analyses. see above). and clade b.0 (Schmidt et al. For this purpose.000 permutations of parasite haplotypes among populations (Excoffier et al. 1992). considering Tamura and Nei distance method (Tamura & Nei 1993). We also analysed variation in the spatial distribution of lineages in relation to hunting management models in host populations. as determined using the Akaike Information Criterion (AIC) implemented in Modeltest 3. The statistical significance of genetic variation was estimated using Monte Carlo simulations with 5.7 (Posada & Crandall 1998). and (2) differentiation among game estates with released birds (sites B. reichenowi AF069610) as outgroups to root the tree.14.Capítulo 4 sequences (Plasmodium vivax GenBank accession no. see below) and the type of hunting management 119 . under a gamma distribution with α = 0. and P. and D). The statistical support for internal branches of the tree was estimated by 1. we conducted a heuristic search and using a tree bisection reconnection (TBR) algorithm for branch swapping. To build the ML tree. and C) and those that maintain only natural wild populations (A. We used analysis of molecular variance (AMOVA. with random addition of sequences. which was estimated from the data by Tree-Puzzle 5. Following the reasoning described above. AF069619.000 bootstrap replicates. Plasmodium malariae GenBank Accession nº AF69624. and built a log-linear analysis with two-factors. showing variable differences (between 0.0 1. Malaria (Plasmodium sp. Table 1.9 Two of the haplotypes found in red-legged partridges (SGS1 and GRW11) have been previously recovered in other avian hosts.7 1.3%) with any known Plasmodium cytochrome b lineage recovered 120 . Plasmodium sp.4 % of prevalence in the host population (Table 1). Plasmodium relictum Plasmodium sp.Fabián Casas Arenas Tesis Doctoral (releasing partridges. Plasmodium relictum Plasmodium sp. 2). non releasing partridges). The remaining six haplotypes have never been previously registered in any other avian host. There were no insertions or deletions.7 D 11 1 1 0 2 0 0 0 29 15 51. Plasmodium sp. and total prevalence within each population studied. which represent an overall 46. Number of birds captured Number of infected birds Percentage of infections Lineage ARF1 SGS1 ARF3 ARF5 ARF6 ARF7 GRW11 ARF9 GenBank EU395835 AF495571 EU395836 EU395838 EU395839 EU395840 AY831748 EU395841 A 11 7 0 1 1 1 0 0 39 21 53.8 B 2 3 0 0 2 0 2 0 35 9 25.9 25. All analyses were done using Statistica 6. were absent in our sample set. Data shown as percentage of infected birds by lineages. and thus the nucleotide alignment was unambiguous.6 1.) parasite lineages recorded within 112 samples of red-legged partridges in four study sites in central Spain. RESULTS Malaria infections were detected in 52 individuals out of 112 Red-Legged partridges screened from 4 study areas.7 Prevalence (%) 51. All parasite cytochrome b lineages examined correspond to Plasmodium spp.9 5. (Fig.9 9. Plasmodium sp. Eight unique Plasmodium cytochrome b lineages were defined by 43 variable nucleotide sites.7 C 3 2 0 0 0 0 1 1 9 7 77. Populations Parasite taxon Plasmodium sp.2% and 2. whereas sequences belonging to Haemoproteus spp.9 1.1 software (StatSoft 2002). Finally. 2). we tentatively consider these lineages as belonging to the same species (P. 2007). at least. The remaining four haplotypes (ARF3. relictum clade and then. All phylogenetic analyses supported this cluster as a sister-clade of Plasmodium relictum sequences (clade b. Furthermore. Other tree reconstruction methods (NJ and MP) produced the same topology. however.Capítulo 4 in avian hosts. and thus may be considered anecdotical infections by lineages depending on other host species (Bensch et al. ARF5. followed by SGS1 (25%). three well differentiated species (Bensch et al. reichenowi (Escalante et al. Three of the haplotypes found (ARF1. lineage ARF7 exhibited much larger differences with respect to all other lineages (range 6. Our isolates SGS1. and GRW11 (5. Sequence divergence between lineages varied from 0.6%). problems with this reasoning in the discussion). Malaria lineages of red-legged partridges Although we did not have morphological data of parasites found by molecular methodology. 2). 121 . 2004). ARF3. Fig. ARF3. which did not contain sequences of any of the morphospecies included in the analysis. our isolates ARF1. which supported the existence of three separate groups of lineages. falciparum and P.7%). according to the sequence divergence matrix our lineages seem to correspond to. ARF5. ARF7 did not match any described morphological species and was placed in the resulted phylogeny close to Plasmodium rouxi species.8% (ARF7/ARF3). and ARF6) clustered together into a well-supported clade (clade a. 2) assuming a GTR+I+G model of nucleotide substitution.7. ARF7 and ARF9) were only detected in single individuals (1. 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. This divergence among potential species was also supported by the phylogenetic relationships between cytochrome b lineages. GRW11 and ARF9 did fall together into the P.9 % of detected haplotypes). 1998).86 %). We built a ML tree (Fig. Fig.7 . The most common lineage in our samples was ARF1 (52% of detected haplotypes). thus corresponding to a very different species.2% (1-bp substitution between SGS1/GRW11 and ARF2/ARF9) to 7. relictum) for further analyses. and ARF6 were pooled together for statistical analyses (see. ARF6 (9. Likewise. malariae GenBank accession no. with 77 % of birds infected. suggesting a differential probability of transmission of lineages among populations. see Table 1). 3). lineage ARF1 clearly dominated the parasite community in three of the four populations studied. reichenowi GenBank accession no. The tree was rooted with sequences from three primate malaria species (P.3.Fabián Casas Arenas Tesis Doctoral Figure 2. clade b. although a large between-population variation in the occurrence of each lineage was observed (see Fig. AF069619. Maximum likelihood phylogenetic tree showing the phylogenetic position of malaria parasites found in red-legged partridges sampled in central Spain (four populations). AF06961. and P. vivax GenBank accession no. The frequencies of the eight lineages isolated in red-legged partridges were not randomly distributed among sampling sites (Table 1. Results derived from ML analysis of cyt b sequences (479 bp) under the GTR+I+G model of nucleotide substitution. The highest parasite prevalence was found at site C. Variations in lineage distribution among populations We found red-legged partridges infected by Plasmodium in all the four sampled populations. Even when considering only lineages present in all the four 122 . Support to internal branches based on bootstrap replicates is indicated by numbers when larger than 50% (1000 replicates). Among infected birds. and lineage ARF7) are indicated by colours as those in Fig. P. Sequences grouped in clades that should correspond to different parasite species (clade a. AF069624). Published sequences of other Plasmodium and Haemoproteus species (GenBank accession numbers are indicated in the tree) have been used to construct the phylogeny. whereas “site B” had the lowest (26% of birds infected. 3). Fig. and 3 to 14 for clade a). There was no geographic structure (n = 4 populations) in the genetic variation of lineage parasites belonging to clade b (P. 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.036). the log-linear analysis of prevalence according to the type of hunting management (releasing partridges vs.17. relictum) (AMOVA: ФST = -0.008). 57% in population A. that reached higher occurrence in game estates without introduced farm-reared partridges than in game estates with releases (Fisher exact P = 0. and 43% in C. large differences in the relative frequency of occurrence among host populations were apparent (Fig. Furthermore. but was absent in game estates without restocking with captive-bred game birds. 123 . Infections corresponding to parasites from clade a represented 93% of total infections in population D. the frequency of occurrence also varied among game estates. although results were non-significant.44.001. P = 0. These findings suggest that human introduction of red-legged partridges in the field is an important factor affecting parasite distribution at local scale. P = 0. estimated genetic variance among populations = 0). 44% in population B. as it was less frequently found in game estates without releasing activity than in sites with releasing activity (Fisher exact P = 0. and considering isolates from the same clade as belonging to the same species.Capítulo 4 sampling sites (ARF1 and SGS1). Fig. for example. comparisons involving populations A and B resulting in nearly significant ΦST value (P = 0. 3). 3). Tentatively.09). possibly as a consequence of small sample size (population D. These differences resulted significant for parasites belonging to ‘clade a’. Fig. the commonest haplotype (ARF1) showed higher occurrence in non-restocking populations than in bird-releasing populations (Fisher exact P < 0. while only 38% and 7% in game estates A and D. see Table 1). while ‘clade b’ followed the opposite pattern.04). had only one sequence belonging to clade b. Indeed. respectively. ‘clade b’ representing the 55% and 57% of infections in game estates B and C. 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. In contrast. Such a tendency of geographic structure depending of the releasing activity was also evident from the pattern of pairwise tests of population differentiation.3). 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 (25.96. non releasing partridges) and parasite clade produced a significant model (partial association: χ² = 6.01. df = 3.38%). Fabián Casas Arenas Tesis Doctoral When population D (n = 1) was excluded from the analysis. Spatial distribution of malaria lineages found in resident red-legged partridges in central Spain. The relative frequencies of the two clades with good support in phylogenetic analyses are represented by histograms (colour-coded as in Fig. the two populations with larger sample sizes (n = 8 and n = 5). and (2) differences in local distribution of lineages among populations of a single host species. P = 0. Lineage ARF7 (yellow bar) is present in only one population. population pairwise ΦST value became significant between populations A (without introduced partridges) and B (with farm-releases birds) (pairwise ΦST = 0.01). or a possible negative consequence of human gamebird releases. 124 . Figure 3.17. 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. which may be indicative of a differential effectiveness in malaria transmission between areas. 1). DISCUSSION We obtained two main interesting results on relevant issues in the study of hostparasite systems: (1) an unusual high prevalence of Plasmodium in resident hosts inhabiting open Mediterranean landscapes.2 to help identification). However. we can not discard a possible real increase in parasite prevalences along last decades. This pattern is now open to debate as a result of the use of molecular techniques to examine parasite infections.6 %. 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. genetic identification). 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. less than 15 % of lesser kestrels Falco naumanni infected by malaria parasites (Plasmodium and Haemoproteus) in central Spain (La Mancha).Capítulo 4 In the only previous studies about hemoparasites in red-legged partridges. but markedly higher than those recorded in birds living in open and arid environments. to differences in the detection efficacy of research protocols (blood smears vs. and often near 0 (Little & Earlé 1995.g. in farmed birds. and Millán et al. Furthermore. For example. 2003). Encinas (1982) found a lower prevalence of P. an area nearby to our study area and with similar landscape features. 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). (2003) found 10 % of prevalence of Haemoproteus spp. Our findings at this 125 . (2007) found. 2004). Earlé & Little 1993). holding the host populations low levels of parasitism more readily found by molecular techniques than by microscopic examination of blood smears (Waldenström et al. using the same diagnostic protocol than this study. The large differences in malaria prevalence between these studies on the same host could be due to different infestation rates between areas. Wandelström et al. Studies on bird species living in open arid or semi-arid environments have detected hemoparasite prevalences usually lower than 20 %. due to an effect of widespreading game releases (see below). Ortego et al.2-16. depending on the sampling method). developed by the classical technique of identifications in blood smears. or may be indicating that wild partridges are locally well adapted to Plasmodium parasite community. 2004). 2004). relictum in wild birds of western Spain in the late 70s (3. Valera et al.g. some recent studies using molecular techniques still reported low prevalences in birds of arid environments. which usually provide higher prevalences than the traditional microscopic examination of blood smears (e. Contrary to this pattern. The lesser kestrel is a migrant and colonial breeder that should theoretically reach higher prevalences than our hosts (resident and territorial). 2006. for example. such as different immunological capabilities of the hosts or different virulence of lineages sampled (de Roode & Read 2003). see e. 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 (PérezTris & Bensch 2005). and ARF6) were broadly distributed among the populations studied. 2005). Finally. 2007). Loiseau et al. as also suggested by spatial distribution of lineages (see below). Three lineages (ARF1. Genetic diversity may affect the ability of species to evolve resistance to malaria (Foster et al. at least partially. different parasite lineages cause different mortality rates among infected individuals reducing the abundance of alive birds with a given lineage (Bensch et al. whereas four lineages were restricted to single populations. Indeed. SGS1. or if the immune system of hosts responds in a different way to each lineage. 2004. or different mortality rates among infected individuals (Bensch et al. 2008) that could help explain differences in susceptibility to 126 . within-host competition among closely related parasites (Martinez-Abrain et al. Pérez-Tris & Bensch 2005. broad geographic range and a probable high potential for local adaptation (described for SGS1. 2007). 2006). Larger scale studies are urgently required to explore this possible negative influence of that management technique.g. Other factors could also underlie differences in parasite prevalences among different host-parasite assemblages living in similar landscapes. to an ongoing increase in prevalences of haemoparasites in wild partridges due to widespread farm-bred partridge releases over the last decades. and Bonneaud et al. We have detected a non-random distribution of Plasmodium lineages infecting hosts from different populations. 2007). Such a result might also be attributed to the relationship between parasite pathogenicity and host resistance if. suggesting low host-specificity for these lineages. and recent studies have found important associations between malaria and MHC genes (Major Histocompatibility Complex) of their hosts (Westerdahl et al. we can not discard that the high prevalence we have found may be due. population density of hosts (but see Keymer & Anderson 1979).Fabián Casas Arenas Tesis Doctoral 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. Bonneaud et al. 2005. de Roode et al. two of the haplotypes found in red-legged partridges (SGS1 and GRW11) have been previously recovered in other avian hosts. maybe jeopardizing other host’s life history traits. and enhancing the possible negative influence of human intervention. and considered the same species in our analyses. the situation could be even worse than the one we are reporting. would induce new immune challenges in wild bird populations (de Roode et al. function as ongoing sources of infection for other individuals or species. the adverse effects of releases for local genetic diversity of parasites are likely to go unnoticed. and humans routinely serve as dispersal agents (Mack et al. 2005). in turn. and taking into account the observed differences in malaria distribution between natural host populations and those managed by humans. Like free-living organisms. 2000) creating novel habitats for parasites that. A human-induced increase in prevalence or diversification of parasite community. and the potential effect of introduction of parasites into new environments should not be discarded. Bensch et al. on the contrary. should be increasingly considered in evolutionary studies.4% in the cytochrome b sequence. in any case. dispersal rates and the choice of breeding places. specially in released farm-bred birds (Alonso et al. particularly in species such as red-legged partridges that are sedentary territorial animals showing only short range movements and dispersal (Del Hoyo et al. 2004). since it is probable that lineages isolated in this study. 1994. at least in resident hosts with low dispersal rates. For example. Management implications 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. humans are 127 . Differences in malaria prevalence between nearby sites suggest that infection probability may depend to a greater extent on factors such as natal site. authors. highlighting the importance of horizontal transmission at local scale. 2005). that low-scale distances and relationships among host populations should be more carefully considered in future studies of host-parasite complex. Gamebird releasing is a very usual activity in many places of the world. 2008 for a recent review). Thus. Under these circumstances. alien (human-introduced) parasites may intensify disease impacts on populations. parasites and pathogens can colonize and evolve in new environments.Capítulo 4 infections between populations of the same host. Such pattern of malaria distribution at local scale demonstrate. could in fact correspond to different malaria species (cryptic species may differ by just 0. such as red-legged partridges. In our case. unpublished data). as well as other closely -related lineages found for first time in this study. We have found. van Riper et al. We also are very grateful to the game managers for permission to work in their hunting lands. 2007). the effects could also be extended to sympatric species. some of which may be under conservation concern (Villanúa et al. Indeed. This project was financed by CYCIT project CGL200406147-CO2/BOS. Casas) and CSIC-I3P (M. Calero-Riestra) grant programmes. whereas the opposite pattern was found for malaria lineages not detected previously in other avian hosts. due to the consequences of the first exposure of native birds to infections (Van Ripper et al. 1995). leaving dramatic examples of bird extinctions on islands (Warner 1968. 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. and the JCCM (F. infected more hosts in areas where game-releasing activity is performed than in wild populations. GRW11). ACKNOWLEDGEMENTS We thank Inés Sanchez and Pedro Gomez de Nova for their help in the laboratory of the IREC. Pérez-Tris during the manuscript preparation. Evidences concerning the effects of blood parasites in wild non-passerine birds are however limited. Tens of million gamebirds are released yearly in Europe (Viñuela & Arroyo 2002). strongly suggest that the potential effect of releases promoting introduction of parasites into new environments should be more carefully considered. for the first time.Fabián Casas Arenas Tesis Doctoral responsible for the introduction of mosquitoes and associated pathogens in different countries. This article benefited from comments and suggestions provided by J. 1986. evidence suggesting the influence of game-releasing activity in malaria spatial distribution at local scale. JT Garcia was supported by a CSICI3P post-doctoral contract. Atkinson et al. Our results indicates that common malaria lineages detected in other bird species (SGS1. 128 . and in red-legged partridges absent. Atkinson & Van Riper 1991). and our results with blood parasites. and further studies are urgently required. by JCCM project PAC06-0137-2179. 1986. 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. as well as previous works with intestinal parasites. J. S. V. Pérez. & Pinheiro.S.L.W. Molecular Ecology 17.F. W. 2048. M. Atkinson. & Parchman. Bensch. M. 1683-1696. dispersal and home range of autumn-released red-legged partridges (Alectoris rufa). Pérez-Tris. J. (2000). Bensch. Bensch. Leucocytozoon (Apicomplexa: Haemosporida) and Hepatozoon (Apicomplexa: Haemogregarinidae). 267 1583-1589.. R. evolution. Journal of Natural History 22. J.. Y. (1991) Pathogenecity and epizootiology of avian hematozoa: Plasmodium.. Hansson. Zuk M).A. B.. M. H.T.. Loye JL. (2004) Linkage between nuclear and mitochondrial DNA sequences in avian malaria parasites .C. C. Jonzen. Waldenstrom. Benkman. In: Bird-parasite interactions: ecology.. A. & Van Riper.A. Proceedings of the Royal Society of London B.. Jhala. Ishtiaq. Hasselquist.. A. 129 . Proceedings of the Royal Society of London B. Journal of Animal Ecology 76. 401-406.T. (2008) The local introduction of strongly interacting species and the loss of geographic variation in species and species interactions.. Westerdahl.. S. Melo. Systematic Parasitology 29.T..S. British Poultry Science 46. Parasitology 111. S. R. Sileo. & Fleischer.. Warren. B. J.. Graves.R. Westerdahl.A. Ostman. Diéz..H. K. (1988) Morphological form in the avian Haemoproteidae and an annotated checklist of the genus Haemoproteus Kruse. C.. M. Atkinson.. H. 29352944. Fonseca. J. & Hasselquist. Gaudioso.. L. R.. Bensch. Peirce MA & Earlé RA (1994) An annotated checklist of the valid avian species of Haemoprtoeus. 1617-1621. Biology Sciences 273.M.R. 112-122.. G. and Haemoproteus.. D. (2006) Global Phylogeographic limits of Hawaii’s avian malaria.. M. Covas. N. Peirce. J.multiple cases of cryptic speciation? Evolution 58.R. B.E. and behaviour (eds.V. C. (1995) Wildlife disease and conservation in Hawaii: pathogenicity of avian malaria (Plasmodium relictum) in experimentally infected Iiwi (Vestiaria coccinea). O.. Siepielski. R. D. & Hellgren. & Peirce. S59-S69. G. pp. & Iko. C.. Host specificity in avian blood parasites: a study of Plasmodium and Haemoproteus mitochondrial DNA amplified from birds.T.. R. Atkinson. Bennett. C.M. (2005) Study of survival.. Woods.A. O. Stjernman.Capítulo 4 REFERENCES Alonso.M. Sejberg.L. Beadell. 61-73. Waldenström. S.. C. Oxford University Press. Dusek. III. New York.. T. 1890. Bennett GF. D. & Prieto. Rahmani. Hansson.. Leucocytozoon. 395-404. F. (2007) Temporal dynamics and diversity of avian malaria parasites in a single host species..J.. (1994) Handbook of the Birds of the World. A.. Pansini.Fabián Casas Arenas Tesis Doctoral Bonneaud.. C. Fallon. (2004) Field interbreeding of released Farm-reared red-legged partridges (Alectoris rufa) with wild ones. S. Trends in Ecology and Evolution 18.. 130 . Vol. R.. A. Walliker.E. 7624-7628.. after the malaria genomes. tomo I.. Garrido..E. Huijben. A.. D. Cheesman.E. B. Pérez-Tris. (2002) Capturas de perdiz roja (Economía inducida por la caza de perdiz)...R. & Ricklefs.E. R. M. 60-61. 141-147. W. Lal. 269-306. J.. & Read. FEDENCA. (2005) Host specialization and geographic localization of avian malaria parasites: A regional analysis in the Lesser Antilles. D.M. Helinski. J.. En: Aportaciones a la gestión sostenible de la caza.. Chan. Proceedings of the National Academy of Sciences of USA 102. C. pp.S. Chastel.L. J.. A. (1993) Haematozoan infection of eight gamebird species (galliformes) from four sites in southern Africa.K. A. & Fleischer.C. II. Collins. Escalante. Duffy.E.A. Duarte. (1982) Plasmodium relictum y P. Palmer.H. L. Molecular Ecology 16. 55-61. J. R.. Bell. R. L. A. P.. Eggert.. S. & Sorci. Evolution 60. Federico. A. J.T. E. Gortázar.E. Genetics 131. & Martín. 466-480.C.L. Earlé. (2007) Genetic structure and evolved malaria resistance in Hawaiian honeycreepers.. & Little. G. Hart. O. Villafuerte. & Sargatal.C. J. 383-389. Foster. Woodworth. R. Wargo. de Roode. J. Smouse. Barcelona. Excoffier. & Vargas.H. Birmingham. (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. J. 4738-4746. Suid-Afrikaanse tydskrif vir natuurnavorsing 23.. Proceedings of the National Academy of Sciences of the USA 95. (1998) The evolution of primate malaria parasites based on the gene encoding cytochrome b from the linear mitochondrial genome.. B. M. Spain. 479-491..J.J.F. 8124-8129.. & Quattro.M. (2005) Virulence and competitive ability in genetically diverse malaria infections. J.M. 112-114. A. Elliott. Madrid.F. cathemerium en Aves del área salmantina. Encinas.A. de Roode.. R. & Read. Zeitschrift für Jagdwissenschaft 46. (2000) Success of traditional restocking of red-legged partridge for hunting purposes in areas of low density of northeast Spain Aragón.A. P. Lynx Ed. S. Freeland. D.. Del Hoyo. Revista Ibérica de Parasitología 42. Game and Wildlife Science 21. American Naturalist 165. D. J. 23-30.C. P.M. (2003) Evolution and ecology. (2006) Major histocompatibility alleles associated with Local resistance to malaria in a passerine. J. P. Evolution and Behaviour. M.. 195–207. Zoorob. W. B. Simberloff. Parasitology 134. Journal of Parasitology 95. Hall.D.Capítulo 4 Gortázar. A. H. P. (2006) Phylogeographic structuring of Plasmodium lineages across the north American range of the House finch (Carpodacus mexicanus). A. 95-98. Oxford University Press. & Zuk. R. (2008) Antagonistic effects of a Mhc class I allele on malaria-infected house sparrows..A. R. W.F.. 219-224. & Schall. M. Loye..E. A.. Ecology Letters 11 (3). 131 . Mack. Loiseau.J. Waite. F.. J.. T. Ecological Applications 10. Hagemeijer. Evans. (2002) The Ecology of Wildlife Diseases. Hudson. Little.L. (2000) Parasite adaptation to locally common host genotypes. Villuendas. Rizzoli.G. 8187. & Vicente. Oxford. & Bazzaz.. Nucleics Acids Symposium Series 41. & Anderson. Nature 405.M.A. Acevedo. Kimura. Poyser. (1995) Sandgrouse (Pterocleidae) and sociable weavers Philetarius socius lack avian Haematozoa in semi-arid regions of South Africa. (2006) Disease risks and overabundance of game species European Journal of Wildlife Research 52. 1043-1049... Keymer.E.. E. Juillard. & Blair. M. & Dobson.A. C. C. & Dybdahl. & Zuk. R. 367–370. M. 384-387. Birad.M. Martinsen. (1997) The EBBC Atlas of European Breeding Birds: Their distribution and abundance.A.. E.M. 483-490. (1999) BIOEDIT: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Hamilton.M. 679-681.S.J.P. Heesterbeek. & Oro.J. Grenfell. (1991) Bird-Parasite Interactions. epidemiology. Clout. Bartolmé. R. D. Lively. Martínez-Abraín. Parasitology 79. & Lovette. Environmental Conservation 31. Lonsdale. G. Ruíz-Fons.D. Oxford University Press. M. M. J. 689-710. E. H..J. M. B. D.T. Journal of Arid Environments 30. (2004) Unforeseen effects of ecosystem restoration on yellow-legged gulls in a small western Mediterranean island. (1982) Heritable true fitness and bright birds: a role for parasites? Science 218. S..J. and control. 258-265. T. (2000) Biotic invasions: causes. P. I. A. (1979) The dynamics of infection of Tribolium confusum by Hymenolepis diminuta: the influence of infective-stage density and spatial distribution. Minués. R. & Earlé. (2007) Morphologically defined subgenera of Plasmodium from avian hosts: test of monophyly by phylogenetic analysis of two mitochondrial genes. Dhondt. & A. J. C.. J.N. London. F.. Federici. Oxford. Sarzo. & Sorci.A... global consequences.. E.M. Ecology. A. Bonneaud. UK. A comparison of the helminth faunas of wild and farm-reared Red-legged Partridge. In. Martín-Mateo. J. Ecology Letters 8. O'Brien. (2004a) Comparative survey of the ectoparasite fauna of wild and farm-reared red-legged partridges (Alectoris rufa). J. Geidelberg. J. E. 132 . 701-707. Hasselquist.P. Price. 838-845.. Møller. Pérez-Tris. Trends in Ecology and Evolution 3. E. Gortazar... Molecular Ecology 17. R.. C. & Villafuerte. Bioinformatics 14. Cordero. J. Pérez-Tris. Hellgren. D.P. Randi. Gortázar. & Villafuerte. 2507-2510. Moreno. (1998) Population limitation in birds. K. D. M. J. I. S. S.Fabián Casas Arenas Tesis Doctoral Merino. Sanz.. Newton. (2007) Genetic characterization of avian malaria (Protozoa) in the endangered lesser kestrel.. e235. Moore J) pp... Abstract of the 4th Sciencific meeting of European Association of Zoo. & Bensch. (1980) Evolutionary Biology of Parasites. (1998) MODELTEST: testing the model of DNA substitution.. & Aparicio.A.105-127. (1988) Interactive influences of infectious disease and genetic diversity in natural populations. (1997) Parasitism and the evolution of host life history. (2008) Detecting hybridization between wild species and their domesticated relatives. 605-611. 817-818. S.M.F. Host-parasite evolution: general principles and avian models (eds Clayton DH. NJ. & Bensch. J.J. Križanauskienė. Fjeldså. 1153-1156.W. & Crandall. S. Proceedings of the royal society of London Series b: biological sciences 267. Germany. Parasitology Research 93. Ortego. G. P.J.. (2005) Dispersal increases local transmission of avian malarial parasites. C. Millán. C. Parasitology Research 101. Journal of Wildlife Management 68. Princeton University Press. J. (2003) First record of Haemoproteus sp. A. Posada. (2007) Within-Host Speciation of Malaria Parasites. Princeton. & Evermann. with an ecological study in wild populations.. Oxford University Press.. C. Calabuig. J. & Arriero. Millán. A. Secondi. (2004b). J. Gortázar. Plos One 2. parasiting Red-legged partridges (Alectoris rufa). Millán. & Villafuerte. 254259. Falco naumanni. J. Oxford. J. J. London. 285-293. Academic Press Limited.and Wildlife Vaterinarians AND European Wildlife Disease Association....J. P. R. O. (2000) Are avian blood parasites pathogenic in the wild? A medication experiment in blue tits (Parus caeruleus). J. Waldenström. R. T. Thompson.. G.. 4673-4680... & Bernatchez.. A.B. (2008) Evolutionary change in human-altered environments. Vingron. C. L. 885-892. 47-60. Goff. O. 209-213. Tamura. T.com. (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. with a description of Plasmodium (Novyella) ashfordi sp. S. J. F. E. M. (2002) Diversification and host switching in avian malaria parasites. D. Barbosa. S. Zehtindjiev. (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment trough sequence weighting. Journal of Arid Environments 55. D. H. García de la Morena.A. Sinauer. M. M. Proceedings of the Royal Society of London Series B: Biological Sciences 269. C.. Morales. Higgins.L. (1986) The epizootiology and ecological significant of malaria in Hawaiian land birds.L.M. J. Molecular Biology and Evolution 10. M. 32-41. Villanúa. Ekologija 1. D. 512-526. Smith.statsoft. Nucleic Acids Research 22.D. Valkiūnas. Gortázar. A negative effect of red-legged partridge Alectoris rufa releases on steppe bird conservation? Ibis 149.0 b10.. version 4. & Nei. S. version 6.G.. Tella. C. (2002) STATISTICA data analysis software system. other methods. Ilieva.Capítulo 4 Ricklefs. 133 . M. R. Schmidt. Sunderland. StatSoft.. K.B. Strimmer. Bioinformatics 18. T. Parasitology Research 100. & Laird. 1311-1322. Iezhova..M. & Bensch. MA. F. Valkiūnas. M.. weight matrix choice.. Viñuela. & Moreno. Valera. & von Haeseler. Ecological monographs 56. (2003) Low prevalence of haematozoa in Trumpeter finches Bucanetes githagineus from south-eastern Spain: additional support for a restricted distribution of blood parasites in arid lands.L. (2007) First occurence of Eucoleus contortus in a little bustard Tetrax tetrax. (2007) Linkage between mitochondrial cytochrome b lineages and morphospecies of two avian malaria parasites. E.L.G.. (2002) The evolutionary transition to coloniality promotes higher blood parasitism in birds.E. Journal of Evolutionary Biology 15. Inc. www. & Gibson. (1993) Pathogenic influence of haemosporidians and trypanosomes on wild birds in the field conditions: facts and hypotheses. 405-406. (2002) PAUP*: phylogenetic analysis using parsimony. P. 502-504.A. Molecular Ecology 17. van Riper. & Fallon.J. G. Carrillo.. K.. (2002) TREE-PUZZLE: maximum likelihood phylogenetic analysis using quartets. nov. parallel computing. Hellgren. Swofford. 327-344. 1-8. A. Casas. position-specific gap penalties. van Riper. J.. T.. Waldenström. Hasselquist. S. & Östman. Westerdahl. P. D. B. U. & Bensch. Belgium. (2006) The Hitchhiker’s guide to avian malaria. L. S. Hansson. & Arroyo.. V. DOI 10. Viñuela.L. Brussels. (2005) Associations between malaria and MHC genes in a migratory songbird. Wood. & Cosgrove. Ö. 134 . (1968) The role of introduced diseases in the extinction of the endemic Hawaiian avifauna. D. Alzaga. F.. Viñuela. REGHAB project.E. Journal of Parasitology 90. recommendations and future research priorities. Hasselquist.. B.. Waldenström. S. C. Acevedo. J. R. C.Fabián Casas Arenas Tesis Doctoral Villanúa.J. Hasselquist.. 1511-1518.. Kiboi.. Gamebird hunting and biodiversity conservation: synthesis. J. von Schantz. Casas. S. & Gortázar. D. J. 1545-1554.. final report. M. Warner. Condor 70.. Proceedings of the Royal Society of London B. European Journal of Wildlife Reseach. Bensch. European commission. & Ottosson.1007/s10344-007-0130-2.. 101-120. Pérez-Rodríguez.. J. Bensch.. 5-7. (In press) Sanitary risk of red-legged partridge releases: introduction of parasites. Waldenström. D.. 191-194. (2002) Crossspecies infection of blood parasites between resident and migratory songbirds in Africa. Trends in Ecology and Evolution 21. J. Biology Sciences 272. (2002). Molecular Ecology 11. H. (2004) A new nested PCR method very efficient in detecting Plasmodium and Haemoproteus infections from avian blood. F. Effects of hunting on the behaviour and spatial distribution of northern lapwings. Journal of Applied Ecology. ..CAPÍTULO 5 Efecto de la actividad cinegética en el comportamiento y la distribución espacial del avefría europea. J. & Bretagnolle. en evaluación. Viñuela.. chorlito dorado y sisón común en el oeste de Francia: Importancia de los refugios de caza en áreas agrícolas Casas. golden plovers and little bustards in Western France: Importance of hunting-free refuges in agricultural areas. V. Mougeot. F. . 4. date and group size. 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. date and group size. and it has received increasing attention given its social and economic dimensions. We took into account variation due to time of day. hunting activity increased flight probability and time spent vigilant (higher on hunting days than just before and after a hunting day). All three studied species showed behavioural responses to hunting activities. The increase in human leisure activities has amplified the potential consequences of human disturbances on wildlife. Departures of little bustards towards their wintering quarters could to be associated with the occurrence of hunting. Hunting is one of human activities that affect most wildlife. Fox & Madsen 1997. This implies greater energetic costs on hunting days. We compared the use of hunting free areas and the behaviour (time spent flying. Hunting-free reserves for game species are zones where birds find an area of reduced disturbance. We also monitored the hunting effect on the migration pattern on little bustard. INTRODUCTION Animals can perceive humans as potential predators and often alter their behaviour in the presence of people. Most studies have been conducted on coastal and wetland areas. including wild birds (Stockweel et al.Capítulo 5 ABSTRACT 1. while the little bustard is fully protected since 1972. golden plovers and little bustards. We also found distributional (use of hunting-free reserve) responses to hunting activities. Also these birds inhabit agricultural areas that are of conservation concern. Arroyo & Razin 2006. during and after hunting took place. to the detriment of resting. 2006). 2. Synthesis and applications. 5. Little bustard almost never left the hunting reserves. The increase in human population and leisure activities has amplified the potential consequences of human disturbances on wildlife (Blanc et al. vigilant. 2006). Holmes et al. 3. An important measure to reduce hunting effect on little bustard migration pattern could be to delay hunting until birds have left the area. in all studied species. After controlling for variations in behaviour due to time of day. Management planning should also be integrated internationally for the creation of refuge networks. Hunting activity can affect bird behaviour and distribution and have a fitness cost. 1991. 2005. However. Increasing the size or number of hunting-free areas might be an important management and conservation tool to reduce the impacts of hunting activities. Lapwings and golden plovers used the hunting reserves mostly when hunting activity took place and other areas when no hunting was conducted. Bautista et al. resting or foraging) of birds on days before. the overall effects of increasing human disturbance on bird populations are 137 . Our aim here is to evaluate the effect of hunting activities on the behaviour and the use of hunting-free areas of lapwings. we show that. The first two species are hunted in France although showing less interest to hunters. Madsen & Fox 1995. 2005. and forest birds. Thiel et al. Robinson & Bennett 2004). hunting reserves where birds can benefit from reduced disturbance have been created in North America and in several European countries (e. 2002). and it has received increasing attention given its environmental. However. Stafford et al. 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. 138 . wetland. Webb & Blumstein 2005). Duriez et al. it is important to take into account the type of disturbance. and references therein). hunting and wildlife conservation (Lucio & Purroy 1992. 2001). the effects that hunting and game management have on non-target protected species are still poorly known (Arroyo & Beja 2002). 2007. Fox & Madsen 1997. Pauli & Buskirk 2007). abundance. and may also affect other species of conservation concern (Madsen & Fox 1995. 2004. Hunting is a widespread human activity. in a context of “wise use”. Because all species do not respond with similar intensity to human disturbances (Blumstein et al. Hunting is perhaps the human activity that affects wildlife most. Several studies (including experimental ones) have shown that birds behave differently in areas with contrasted levels of human disturbance (Fox & Madsen 1997.g. depending on the availability of alternative habitat and the fitness costs of disturbance (Gill et al. adjusting human traditional activities. and is considered one of the main factor behind population declines or extinctions of many species (Newton 1998).Fabián Casas Arenas Tesis Doctoral still poorly documented (Guillemain et al. These studies have evidenced that hunting causes local disturbance effects on target game species. 2003. Hunting activity can however be compatible with a conservationist policy. with two complementary components that directly influence the population dynamics of species: mortality and disturbance (Tamisier et al. Thiollay 2007). Most studies about the effect of hunting disturbance on birds have been conducted on coastal. Bregnballe et al. 2007. Madsen 1998b). In a recent attempt to reduce hunting impact on behaviour and distribution of wildlife. how. 2007. Tapper 1999. Klaassen et al. their frequency. and on effects on behaviour. Fox & Madsen 1997. whenever an adequate management plan is implemented. particularly in Europe (Lucio & Purroy 1992. and that their avoidance behaviour may vary both temporally and spatially. 2005). González et al. and there is often much debate about how human activities must be regulated (see e. and fitness of target game species (Madsen & Fox 1995. social and economic dimensions.g. mainly focusing on waterfowl and game species. 2006. promoting and financing preservation of natural ecosystems. Martínez et al. distribution. 2007). hereafter “golden plover”) and the little bustard (Tetrax tetrax). Hence. In France. agricultural intensification and changes in land use (Bota et al. These species are the northern lapwing (Vanellus vanellus.000 administrative districts (“Communes”). farmland habitats hold c. Thus. 2007). Hunting activity is widespread in farmlands and agricultural habitats (Howard & Carroll 2001. 2005). at least 10% of the surface of the Commune is set as a hunting-free reserve. 80 % of the country’s population of little bustards 139 . are organised into local associations (“Associations Communales de Chasse Agrée” or ACCA) that manage hunting activities since 1991. and that are of conservation concern. Howard & Carroll 2001. but their efficiency as management tools has been poorly investigated yet (Duriez et al. while the little bustard is fully protected since 1972. and should be integrated with agricultural management programs (e. Farmland habitats (agrarian pseudo-steppes) are under increasing pressure because of rapid natural habitat loss. Refuge size. In western France. and on practical methods to reduce the effects that hunting activities might have on species of conservation concern (Tucker & Heath 1994). in most cases hunting is carried out only some days a week. Spain or the U. 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. 2007).Capítulo 5 Madsen 1998a. there is a need for further research on the effects of hunting activities on key farmland bird species. location and network structure must ensure birds find all their biological requirements. 2001. most of these in agricultural areas. Robinson & Sutherland 2002). 2002). 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 hunting is completely prohibited inside these hunting reserves (Trouvilliez 1997). hereafter “lapwing”). This is important because population declines have been reported in many bird species in agricultural habitats (Donald et al.g. Jolivet et al. All these are subject to common rules. but the effects of hunting on birds in these habitats remains little studied as compared with birds inhabiting other habitats.K. the european golden plover (Pluvialis apricaria. 2002). reducing to a minimum the external disturbance (Fox & Madsen 1997). Stafford et al. hunters of approximately one third of the 55. The two former are hunted in France. 2005). Game shooting is one of the main alternative options available to farmers in several European countries such as France. In all ACCAs. Madsen 1998b. Martínez et al. Martínez et al. This activity often provides an added socioeconomic value in some rural areas (Bernabeu 2000. We compared the use of hunting free areas and the behaviour (time spent flying.15%). In 2003. date and group size (for instance. Behaviours might differ depending on the time of day. resting or foraging) of birds on days before hunting took place.g. 2007). which confers international responsibility to protect this population. The habitat within the study area is dominated by intensive agriculture with a mixture of winter cereal (c. Hunters locally targeted small game mammals (european hares Lepus europaeus and wild rabbits Oryctolagus cuniculus) and game birds (grey partridge Perdix perdix. rapeseeds (c. Releases of captive bred partridges and pheasants are a common management tool.Fabián Casas Arenas Tesis Doctoral (Jolivet et al. Béchet et al.15%).50%). by a variable number of hunters. We also investigated whether departures on migration of little bustards coincided with hunting disturbances MATERIAL AND METHODS Study Area We conducted this study in a 340 km² cultivated area in South-Western France (46°37’N. The hunting method used was walk-up shooting with dogs (usually 140 . 1) in October and November 2003. 0°2’W. to the detriment of resting or foraging activities. but see Beauchamp 2001). with pasture and alfalfa being reduced to less than 15%. a threatened species. hereafter referred as to the core study area (Fig. and then the effect of hunting. hunting season was legally opened on 5 of October. and use more often hunting-free areas when hunting takes place. from sunrise to sunset. Fig. 1). Within this area. McNamara & Houston 1992. and would spend more time flying and being vigilant. hunting was conducted twice a week (on Thursdays and Sundays). we studied more intensively a much smaller area (c. sun-flower and maize (c. during a hunting day. so we first investigated the effect of these factors on bird behaviour. vigilant. showing less interest to lapwings and plovers. We also predicted that birds would avoid areas where disturbance due to hunting activities take place. time spent in vigilance is expected to decrease with increasing group size. We predicted that birds would be more often disturbed during hunting days. Hunting activities may affect migratory decisions (e. and after a day of hunting. In this ACCA. red-legged partridge Alectoris rufa and ring-necked pheasants Phasianus colchicus). 2003). 10 km2) located between the villages of Tauché and Sainte-Blandine (“Commune” of Tauché). generally with a break in the middle of the day. Lapwings winter commonly on the study area. captured underground or over soil surface (Shrubb 2007). most birds arriving in OctoberNovember. the hunters forming an attacking line of 3-6 hunters. Lapwings inhabit mainly grasslands and wet farmlands. spaced every c. Golden plovers are less common than lapwings in our study 141 . The golden plover is a medium-size wader wintering on the coast or inland. Location and map of the study area in Western France (commune of Tauché). These are set by local hunters. hunting is permitted in some areas. 1 km Tauché Sainte-Blandine Figure 1. insects and others invertebrates. but not in other. in pasture and arable farmland habitats throughout temperate south-western Europe (Cramp & Simmons 1983). 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 ○). In white fields outside the reserve. 1). but sometimes up to six). Within the study area. 40-50 metres. Study species The lapwing is a medium-size wader with a widespread palearctic distribution. which act as wildlife reserves (ACCAs) and are most often located near villages (see Fig.Capítulo 5 one or two dogs per hunter. in grey hunting-free area. where they feed on earthworms. We began conducting transects every working day from sunrise until 11. “Vulnerable” in Europe (Goriup 1994) and red-listed in France (Rocamora & Yeatman-Berthelot 1999). 2007). when birds were less active. 1). In western France. For each observation. during and after hunting took place. 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. 2005. Observations were made from a distance such that birds were not disturbed during transects.00 until sunset (pm). Transects were conducted before the start of the hunting season in the core area. we recorded the date. 2002). and when hunters use to have a break.Fabián Casas Arenas Tesis Doctoral area. and on days before. and typically form mixed flocks with lapwings. number of individuals of each species. Transects were not conducted in the middle of the day. The little bustard is a mediumsized Otididae typical of steppic and extensive agricultural habitats. identify and count birds using binoculars or a telescope. obs. birds leaving in early autumn towards their wintering quarters in Spain (Morales et al. and the habitat used. the species is migratory. following a bi-modal activity pattern commonly found in birds (pers. Roth & Lima 2007 and references therein). The observer was driving at low speed (20 km/h) and stopping regularly to look for. see Cope 2003. but in a different order every working day (Fig. The little bustard breeding populations of western France have suffered dramatic declines in recent years (Morales et al. 142 . This species is currently classified as “Near Threatened” at the world level (BirdLife 2000). flock size and habitat use We studied the distribution of focal species using road transects within the core area.00 (am) and between 16. Jolivet et al. Data collection Distribution.. exact location on a map. time. 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. For each observation.00) and flock size (number of birds in the group).Capítulo 5 Behavioural observations When a flock was located. but we tried to sample individuals only once. 1983). which were defined and classified using prior experience and previous works describing the main behaviours of study species (Barnard et al. (4) foraging. and conducted a 60 sec (± 1) focal sampling (see Altmann 1974). The maximum number of observation in a given flock was 20. recorded as the % time spent searching for food (scanning.00-19. with the body. and only when we were confident that it was a different individual. Specifically. we also recorded the following data: sampling date (julian date. lapwing and golden plover.00-12. which served as a hide. 143 . 1982. using stop-watch and a tape recorder.00 or pm. and birds always seemed unconcerned by the presence of the observer. neck and head raised. 26 and 22. 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. (3) resting. lapwing: n = 375. recorded as the % time spent resting or preening when landed. recorded as the % time the focal bird spent vigilant when landed. respectively for little bustard. by switching to another bird that was at least at 10 metres from the previous focal one. and peck leaves while walking (pers. Lapwings and golden plovers are “pause-travel” foragers. golden plover: n = 172. Barbosa & Moreno 1999). Birds were not individually marked. trampling) or feeding when landed. 1= 1st of October). 16. Cramp & Simmons 1980. 9. we randomly selected one individual within the flock. Sample sizes for individual behavioural observations were as follows (n of individual focal samplings): little bustard: n = 298. Recordings of behavioural observations were subsequently analysed to quantify the duration of each behaviour. obs. After each focal sampling. (2) vigilance. subsequently allocated to one of two daytime period (am. vigilant birds adopt a conspicuous upright body posture.). we waited for 1-2 minutes before starting another focal sampling on another bird. Observations were conducted from the car. we recorded (1) the occurrence of flight by the focal bird. time of day. Little bustard eat vegetation in winter. We tested for non-linear relationships with sampling date or group size by including a quadratic term in the model (date2. we conducted pairwise comparisons between days before. When variation in behaviour was explained by hunting activity. day after hunting). hunting day and after hunting day) we included these as explanatory variables in the models. during and after hunting took place. Explanatory variables included the daytime period (am vs pm). To control for variations due to daytime period. 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. day when hunting took place. date. we performed a Chi-square analysis on a contingency table with the variables “reserve use” and “hunting day”. the group size and the hunting activity (three classes: day before hunting. We fitted the variable “reserve use” to the model using a binomial logistic model with log link function. and kept it in our models when significant (P < 0.Fabián Casas Arenas Tesis Doctoral 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. 144 . group size2). the sampling date (julian date). hunting day and day after hunting). flock size and hunting activity (before hunting day.05). The significance of the effects was tested using the Wald statistic (test of significance of the regression coefficient). 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. habitat. 91 3. Non-significant variables (P = 0.283 Little Bustard Chi2 P 9.66 3.043 0.001 <0.34 8.57 6.283 1.283 2. group size and hunting activity on the behaviour of studied species.014 1.026 0.001 df F P 1.283 1.32 <0.70 1.107 0.283 1.24 0.027 <0.08 0.04 7.039 6.001 P 2.006 0.266 1.107 9.04 0.15 F 5.001 P 0.010 0.70 6.Capítulo 5 Table 1.001 0.044 1.290 2.283 1.10 level) were removed sequentially using a backward selection procedure.22 0.266 1.002 Foraging 2.57 0. All initial models included daytime period (am vs pm).266 1.11 0.107 6.693 Vigilance Northern Lapwing df Chi2 P 1.367 6.93 6. date.49 19.26 <0.001 Resting 2.19 5.010 0.283 2.001 <0. Behaviour Flying probability Source of variation Daytime period Group size Group size2 Hunting activity Daytime period Date Date2 Group size Hunting activity Daytime period Group size Group size2 Hunting activity Daytime period Date Group size Group size2 Hunting activity df 1.026 1.684 145 .009 0. group size and group size2 (to test for linear or quadratic relationships with date or group size) and hunting activity (day before.72 <0.266 1.019 0.290 df 1.001 0.53 <0. Effects of daytime period.367 34.290 df 1.37 16.063 <0.93 9.46 F <0.54 4.001 15. sampling date and sampling date2. during or after hunting took place).266 2.367 16.45 15.57 0.53 6.367 4.001 2.283 1.283 1.96 0.012 <0.266 5.38 0.266 4. Only the final models are presented.166 2.033 0.266 4.039 1.266 1.37 <0.001 0.283 1.156 df Golden Plover Chi2 P 11.283 2. but was explained by daytime period (birds were more likely to fly am than pm) and hunting activity (Table 1. 130 = 12.09. Table 1. Flying probability was significantly higher on days after hunting than on days before hunting (F1. sampling date (vigilance increased non-lineraly.001) or after hunting (F1.61. 250 = 6. but increased in larger groups.73. and were also more likely to fly on days after hunting than on days before hunting (F1. peaking at the end of the study period). Variation in the % time spent vigilant by little bustards was explained by daytime period (birds spent more time vigilant am than pm). > 500 individuals) and hunting activity (Table 1.009). 2).77. P < 0.495). 169 = 16. 2). P = 0. 113 = 0.002). Little bustards spent more time vigilant on hunting days than on days prior to hunting (F1. 203 = 29. 92 = 9.46.001).001). P = 0.001) or after hunting (F1. P = 0.Fabián Casas Arenas Tesis Doctoral 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. For lapwings.47.16. flock size (quadratic function: flight occurrence decreased with increasing group size. Time 146 . P < 0. P < 0. Fig.85. 2). 250 = 14. Fig. Time spent vigilant. For golden plovers. Golden plovers were more likely to fly on hunting days than on days prior to hunting (F1. P < 0. 233 = 33. ie. Lapwings were more likely to fly on hunting days than on days prior to hunting (F1.001). P = 0. 2). Fig. flock size (vigilance tended to decrease linearly with increasing group size) and by hunting activity (Table 1. flight probability during a watch was not significantly explained by sampling date. Fig. variation in flight probability was not significantly explained by sampling date or flock size. but not on days after hunting as compared with hunting days (F1. but was explained by daytime period (birds were more likely to fly pm than am). 22. P = 0. variation in the % time spent resting was not significantly explained by daytime period. 190 = 0.772). P = 0. P = 0.37.024).643). For golden plovers.25. 193 = 0. 166 = 14. P < 0. Lapwings spent more time vigilant on hunting days than on days prior to hunting (F1. Golden plovers spent more time vigilant on hunting days than on days prior to hunting (F1. P = 0. Fig. 190 = 0. P = 0.Capítulo 5 spent vigilant did not differ significantly between days before or after hunting (F1. 2). sampling date or flock size. 203 = 16. 87 = 8. Little bustards spent less time resting during a hunting day than on a day before hunting (F1. Variation in the % time spent resting by little bustards was not significantly explained by daytime period or sampling date. P < 0. 2). 2).043).009) or after hunting (F1. P = 0.001) or after hunting (F1.98. For golden plovers. 174 = 6. but time spent vigilant did not differ significantly between days before or after hunting (F1. P = 0. but spent a similar amount of time .87.86. but was explained by hunting activity (Table 1.004).87. but was explained by hunting 147 169 = 10. sampling date.001) or after hunting (F1.001). For lapwings.607). or flock size. 172 = 16. variation in the % time spent resting was not significantly explained by daytime period or sampling date.08. but was significantly explained by flock size (resting increasing linearly with increasing group size) and by hunting activity (Table 1. P = 0.22. but spent a similar amount of time resting on days before and after hunting (F1. and also spent more time vigilant on days after hunting than on days before hunting (F1. variation in the % time spent vigilant by lapwings was explained by daytime period (birds spent more time vigilant pm than am). Time spent resting. 2). P < 0. Fig.001). 66 = 4.001) or after hunting (F1. variation in the % time spent vigilant was not significantly explained by daytime period. Fig. P < 0. resting on days before and after hunting (F1. 191 = 2. 67 = 19. sampling date (time spent vigilant increased linearly with date). Lapwings spent less time resting during a hunting day than on a day before hunting (F1. but was significantly explained by flock size (quadratic relationship: resting increased with increasing group size. 168 = 5.74.55.087).12. flock size (vigilance decrease linearly with increasing group size) and by hunting activity (Table 1. Fig. P = 0.27. For lapwings. but decreased for largest groups) and by hunting activity (Table 1. 6 0.1 0.10 0.65.04 0.Fabián Casas Arenas Tesis Doctoral activity (Table 1.11. P = 0. P = 0.020).08 0. resting and foraging by little bustards. when hunting took place and after a hunting day).339). 148 .92. Fig.06 0. 2).4 Lapwing 0. Mean ± SE flight probability and time spent vigilant.0 60 Golden plover Flight 0.6 0. Golden plovers spent less time resting during a hunting day than on a day before hunting (F1. 87 = 0.1 0. but spent a similar amount of time resting on days before and after hunting (F1.5 0. After hunting Before hunting Hunting day Little bustard 0. 67 = 9.004) or after hunting (F1. 66 = 55.4 0. lapwings and golden plover according to hunting activity (before a hunting day.3 0.0 60 Vigilance 30 20 40 40 20 10 0 50 40 0 50 40 30 30 20 20 10 0 40 10 0 25 30 20 0 50 40 30 20 10 0 30 Resting Foraging 20 20 15 10 20 10 5 0 0 10 0 Figure 2.02 0.2 0. P = 0.2 0.3 0.5 0.00 50 40 0. Hunting and use of hunting-free reserves We found significant differences in the use of hunting reserves before. flock size or hunting activity (Table 1. Table 1). 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). 2).Capítulo 5 Time spent foraging. Variation in the time spent foraging by little bustards was not significantly explained by daytime period. Fig. 120 Before Hunting Hunting Day % of observations within hunting-free area 8 100 8 12 22 After Hunting 80 60 40 17 17 20 0 little bustard lapwing and golden plover mixed flocks Figure 3. but was not significantly explained by flock size or hunting activity (Table 1. 2). 149 . but decreased in largest groups. Fig. df = 2. during and after a hunting day by lapwing and golden plover mixed flocks (χ² = 23.581. 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). Sample size refers to number of flocks. Fig. time spent foraging increased with increasing group size. 2) but was explained by flock size (quadratic function. when hunting took place (stripped bars) and after a hunting day (black bars). For golden plovers. variation in the time spent foraging was not significantly explained by daytime period. For lapwings. sampling date. sampling date or hunting activity (Table 1. 0022. nor by any of the interactions between these variables. 150 .053.35) or habitat (Wald = 2. Fig.846. Flocks were more often found within hunting reserves when hunting took place than when it did not (Wald = 12. Variation in the probability of using the reserve was not explained by flock size (Wald = 0.81). P = 0.17. sampling date (Wald = 0. 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.47). P = 0. 3). daytime period (Wald = 0. Little bustards almost exclusively used the hunting-free area.234. 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.Fabián Casas Arenas Tesis Doctoral P < 0. P = 0. All but one of the observations of little bustards (n = 26) was outside the hunting reserve (Fig. 90 80 70 60 Population Size 50 40 30 20 10 0 1 2 3 4 5 6 7 POPULATION SIZE HUNTING DAY 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 Date Figure 4.001). Seasonal variations (day 1 = 1 October 2003) in the number of little bustard counted on the study area. 4). 60% of the little bustards present in the area) was observed just after the first hunting day (Fig.476.67). 3). P = 0. P = 0. golden plover and little bustard. distribution and migration pattern. something that could be expected given the relatively short study period (two months). or date. This is in accordance with the hypothesis that. Disturbance associated with hunting activity reduced the time spent by birds resting but increased the time spent being vigilant and flying. These differences between two species gathering in common flocks may be related to their contrasted foraging ecology (see Gillings et al. if hunting is a relevant disrupting source. and would avoid areas with disturbances due to hunting activities and use more often hunting-free areas. when they also spent more time vigilant. Clear daily rhythms in activity patterns were also found for lapwings. 2005). Madsen 1998a. This could be a consequence of the start of hunting season. we only found an effect of time of day on flight frequency. The effects of the latter varied depending on the species. Hunting activity affected behaviour.Capítulo 5 DISCUSSION We found that all three studied species showed behavioural as well as distributional responses to hunting activities. Féret et al. while the effect of hunting disturbance was fairly consistent across species. We found few significant effects of sampling date on behaviour. Because we found similar behavioural effects of hunting activity in northern lapwing. Madsen 1998b. after considering other possible sources of variations factors. We found that little bustards and lapwings increased time devoted to vigilance during the study period. 2003). and be related to predators´ daily activity rhythms (Roth & Lima 2007). However. birds would be more often disturbed during hunting days. time of day. given the effects of hunting 151 . revealing that this activity causes disturbance and may induce additional energetic costs (Jarvis 2005). 1996. hunting might similarly affect other birds occupying the same habitat. These results are similar to those found in other species (Riddington et al. we found no evidence that it affected the time spent feeding or foraging. while they spent more time foraging in the morning. higher in the morning. such as flock size. In the case of golden plovers. Factors other than hunting affecting variation in behaviour Little bustard flights were exclusively observed in the morning. Time devoted to vigilance and flights may reflect predation risk. highlighting potential implications at a community level. which were observed flying more frequently and spending more time vigilant in the afternoon. flock size did not influence at all behaviour. time spent vigilant decreased with group size. and would indicate. For lapwings. little bustards need to increase their energetic storage (fat and protein) and food resources can be temporally limited. so flock size should not influence the scan rate behaviour (Barbosa 2002). 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. that birds might not habituate to hunting disturbance. and group size decreased as birds departed on migration. other factors not considered in this study. Lapwings and golden plovers are considered as “pause-travel” foragers (Barbosa & Moreno 1999). while resting increased. 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). Flock size had an important effect on the time spent foraging and resting in the little bustard. When resources are limited. because just before departing on migration. under intraspecific competition. suggesting a trade-off between these two activities. However. both increasing with group size. 1982). but decreasing in largest groups. which may be explained by scramble competition (Beauchamp 2001). In lapwings. 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. at least for little bustards. such as new arrivals and a high turnover of wintering birds. competition for a limited food resource is plausible. Golden plovers may also benefit from Lapwings vigilance in mixed-species flocks. or an increase in foraging proficiency as they become acquainted with food resources in wintering grounds. This could also be because time spent vigilant decreased with group size. however. 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). which may reduce the time spent foraging. could also explain this increase in vigilance.Fabián Casas Arenas Tesis Doctoral on vigilance. flocking thus seem to decrease the proportion of time that each individual spend vigilant (Redpath 1988). In lapwings. while time spent foraging decreased over the same period. In our case. In this species. In golden plovers. 152 . time spent vigilant increased linearly with date. allowing birds to spend more time in other activities. Hunting-free reserves thus 153 . Berthold 2002). Little bustards and lapwings recovered quickly after a hunting day their basal time spent vigilant. In order to save energy. 2003. Béchet et al. Hunting activity and use of hunting-free reserves Little bustards almost never left the hunting reserves during hunting season. such as shorebirds.g. may be because they are more nocturnal feeders than little bustards. Bustards may thus need to forage more during the day than invertebrate feeders. Béchet et al. 2003. golden plovers remained more vigilant after a hunting day. since birds used hunting-free reserves mainly on hunting days and the area around reserve on other days (see below). and this food source is relatively poor (low rates of energy assimilation per unit of mass consumed). suggesting that they might be less tolerant and particularly sensitive to this type of disturbance. Lapwings and golden plovers also spent more time flying after a hunting day.Capítulo 5 Hunting disturbance and behaviour Hunting disturbance caused increased flight frequency and time spent vigilant. 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. 2005). Flying more often and spending more time vigilant to the detriment of resting implies greater energetic costs. birds usually resort to resting. and may be thus particularly sensitive to this kind of disturbance. which implies a higher energy consumption. and in some cases may lead to a greater predation risk (e. Jarvis 2005). These behavioural effects were consistently found in the three studied species. The time spent foraging by lapwings and golden plovers were lower than for little bustard. to the detriment of resting. However. like little bustards. In migratory species. Fat storage rates can be affected by intrinsic (as shedding timing or corporal mass) or extrinsic factors (food availability or predation risk. which can complement their food supply needs at night (Gillings et al. Little bustards are herbivorous in autumn and winter (Cramps & Simmons 1980). 2004. Hunting disturbance might reduce nutrient storage by increasing time spent flying or vigilant (Féret et al. fat storage might be particularly important prior to the migration (Féret et al. 2004). but flight probability increased on hunting days. Berthold 2002). We did not find that time spent foraging decreased with hunting activity. lapwings and golden plovers used the hunting reserves mostly when hunting activity took place. Béchet et al. we found that the first main departure occurred just after the first hunting day. Hunting and little bustard migration pattern Hunting disturbance may not only influences habitat use. As a response to hunting activity. which may be more important for wintering lapwings and plovers than shores). suggesting that hunting may influence migration. like little bustards. M. as found in other birds subject to heavy hunting pressure such as waterfowl (Fox & Madsen 1997. In contrast. Percival et al. but his study focused on migratory waterfowl. Little bustards migrate at night (Morales. Ebbinge 1991. when including adjacent terrestrial habitats into the hunting-free reserves for waterfowl. Duriez et al.. Madsen (1998b) did not find a preferential use of hunting-free reserves by lapwings and golden plovers. more information would be needed to confirm these patterns. change migration routes or wintering areas. but quickly resumed using other areas as soon as hunting stopped. 154 . Bregnballe & Madsen 2004. they could also benefit breeding birds when hunting also occurs during breeding season. 1997. Our findings are consistent with those previous work conducted mainly on wetland and forest game species (e. but also migration patterns. but not in others. In fact. and García de la Morena. E. golden plovers and lapwings moved to non-hunted areas as a quick response to start of hunting activity (Bregnballe & Madsen 2004). 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. Percival et al. In migratory little bustards. if reserves are hunting-free all year round (like ACCAs in France). However. 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. 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. unpublished data). and hunting disturbance the previous day may have stimulated the departure decision.g. 2003). Therefore.Fabián Casas Arenas Tesis Doctoral appeared crucial for this endangered species. Furthermore. birds may migrate earlier. Béchet et al. 2004. 1997. Wolff et al. 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. from complete confinement to hunting-free areas in the case of little bustards. 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. Birds can become habituated to their local level of disturbance. However. 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. 155 . Species confined within hunting-free reserves might have a reduced choice of feeding habitats. at least three caveats to that efficacy could be raised. 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. some species particularly sensitive to hunting disturbance could restrict themselves to game reserves during hunting season. First. we detected some important differences in the level of sensitivity to hunting disturbance. suggesting that hunting disturbance may affect a wide range of species. birds often respond to disturbances as if it was a predatory event. 2001). 2005) which could make them more susceptible to predation (Webb & Blumstein 2005). are particularly important for foraging at this time of year (pers.. For little bustards. 2001).obs. probably because they provide relatively high energy as compared with other available crops. Therefore. Our study showed that hunting caused behavioural changes and displacement of birds from hunting areas to reserves areas on hunting days. becoming more tolerant in more disturbed areas (Blumstein et al. These three species had different life histories and ecological requirements. and it could be useful to replicate this kind of study in areas where reserves have been established for longer periods. crops such as rape-seed or alfalfa. Finally. Second.Capítulo 5 Management implications With the necessary caution when dealing with results obtained at a local level. This was apparent for little bustards in our study. Thus. to movements in and out of reserves depending on hunting activities in the case of golden plovers and lapwings. Game reserves considered in this study were of recent creation (1991). Spain (PAI06-0112). given the predatory and searching behaviour of dogs (Martinetto et al. In any case. Management planning should also be integrated internationally. The way hunting is conducted may thus be adapted to minimize disturbance effects. another alternative might be the payment of incentives to hunters for increasing the size of the hunting-free areas. 2007). especially for migratory species by creating a network of refuges. which are difficult to separate from each other. Jolivet et al. Spain (PAI06-0112). In such cases. 1998. Alex Millon and Diane Desmonts. 156 . if an increase of hunting-free areas is applied as a hunting disturbance buffer. especially to Carole Attié. He thanks the students and researchers at Chizé station during his stay for field work.Fabián Casas Arenas Tesis Doctoral Hunting activity encompasses disturbances by pedestrian (hunters). FM was supported by a NERC advanced fellowship. Spain (CGL 2006-11823) and from the JCCM. a Grant from the Ministerio de Educación y Ciencia. when hunters go with dogs. dogs and gunshots. the main wintering area for little bustards of western France population (Morales et al. An increase in the size of hunting-free areas might mitigate hunting disturbance. Lafferty 2001). Mobile hunting techniques generally cause greater disturbance than hunting from a fixed point (Fox & Madsen 1997). a Grant from the Spanish Ministerio de Educacion y Ciencia. which helped him to do more bearable that time. Additionally. and could be an important management tool. it is important to identify minimum size and threshold levels of disturbance that can to be compatible for hunting activity and conservation. 2002). Loïc Hardouin. Spain (CGL 2006-11823) and from the Junta de Communidades de CastillaLa-Mancha. ACKNOWLEDGMENTS For this work FC was supported by a Marie Curie fellowship of the European Community programme. due their dramatic population declines in recent years (Morales et al. there is a further source of disturbance. since they all occur simultaneously. 2005. FM was supported by a NERC advanced fellowship. This could be particularly important in areas where threatened species as little bustard are present. 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. This could be particularly important in the centre-south of Spain. Journal of Applied Ecology 40. 726-732. D. C. Bernabeu. A.. (2002) Does vigilance always covary negatively with group size? Effects of foraging strategy.htm) European Commission. 712-725. (2003) Changes in vigilance with group size under scramble competition.. 225-267.J. Beauchamp. Thompson. 44-69. Conservation Biology 18 (3). J. 157 . H. Barnard. M. Garcia.D. Giroux. (1995) Foraging strategies and their influence on scanning and flocking behavior of waders. G. Oxford University Press.Capítulo 5 REFERENCES Altmann.. Behaviour 80. J.. (2001) Should vigilance always decrease with group size? Behavioural Ecology and Sociobiology 51. Behaviour 15. Nichols.B.es/irec/reghab/ informes. (1982) Time budgets.uclm. G.. G.B. Universidad de Castilla-La Mancha. (2000) Evaluación económica de la caza en Castilla-La Mancha. 672-675. J. L. A. The Auk 116 (3). B. G. (1974) Observational study of behaviour: sampling methods.. Spain. R. Béchet. The American Naturalist 161. Barbosa. & Moreno. P. Oxford. Bautista. Arroyo. Giroux. Berthold. (1999) Evolution of foraging strategies in shorebirds: An ecomorphological approach.G. & Hines. C. M.L. Béchet. P.M. Biological Conservation 128 (2). Journal of Avian Biology 26 (3). A. (2005) Effect of weekend road traffic on the use of space by raptors. J. A. Barbosa.F. feeding efficiency and flock dynamics in mixed species flocks of lapwings. Palacin.. Barbosa. E.T.E. 689-700.. Beauchamp. Calamaestra. Journal of Applied Ecology 41. PhD Thesis. habitat use and energy of spring staging snow geese.F. (2004) The effects of disturbance on behaviour. J. (2003) Spring hunting changes the regional movements of migrating greater snow geese. & Razin. 47-52. (2006) Effect of human activities on bearded vulture behaviour and breeding success in the French Pyrenees. (2002) Bird migration. & Beja. (http://www. 553–564. Bruselas. 276-284. Morales. B. Report WP2 to REGHAB project. & Viñuela. J.A & Stephens. R. A general survey. & Gauthier. & Ruxton. 51-55. J. A. R. Gauthier. 182-186. golden plovers and gulls. Arroyo. Martin.A. G. Second edition. Bonal. C. (2002) Impact of hunting management practices on biodiversity. Acta Ethologica 5 (1).D. Fabián Casas Arenas Tesis Doctoral BirdLife International. (2000) Threatened birds of the world. Barcelona & Cambridge, UK. Lynx Editions and BirdLife International. Blanc, R., Guillemain, M., Mouronval, J.B., Desmonts, D. & Fritz, H. (2006) Effects of non-consumptive leisure disturbance to wildlife. Revue D Ecologie-la Terre et la Vie 61 (2), 117-133. Blumstein, D.T, Fernandez-Juricic, E., Zollner, P.A. & Garity, S.C. (2005) Interspecific variation in avian responses to human disturbance. Journal of Applied Ecology 42 (5), 943-53. Bota, G., Morales, M.B., Mañosa, S. & Camprodon, J. (2005) Ecology and conservation of steppe-land birds. Lynx edicions & Centre Tecnològic Forestal de Catalunya, Barcelona, Spain. Bregnballe, T. & Madsen, J. (2004) Tools in waterfowl reserve management: effects of intermittent hunting adjacent to a shooting-free core area. Wildlife Biology 10 (4), 261- 268. Bregnballe, T., Madsen, J. & Rasmussen, P.A.F. (2004) Effects of temporal and spatial hunting control in waterbirds reserves. Biological Conservation 119, 93-104. Cope, D.R. (2003) Variation in daily and seasonal foraging routines of non-breeding barnacle geese (Branta leucopsis): working harder does not overcome environmental constraints. Journal of Zoology 260, 65-71. Cramp, S. & Simmons, K.E.L. (1980) The Birds of the Western Palearctic: Hawn to Bustards. Vol. II. Oxford University Press, Oxford. Cramp, S. & Simmons, K.E.L. (1983) The Birds of the Western Palearctic. Vol. III: Waders to Gulls. Oxford University Press, Oxford. Donald, P.F., Green, R.E. & Heath, M.F. (2001) Agricultural intensification and the collapse of Europe's farmland bird populations. Proceedings of the Royal Society of London Series B 268, 25-29. Duriez, O., Eraud, C., Barbraud, C. & Ferrand, Y. (2005) Factors affecting population dynamics of Eurasian woodcocks wintering in France: assessing the efficiency of a hunting-free reserve. Biological Conservation 122, 89-97. Ebbinge, B.S. (1991) The impact of huntinf on mortality rates and spatial distribution of geese wintering in thewestern palearctic. Ardea 79, 197-210. Fox, A.D. & Madsen, J. (1997) Behavioural and distributional effects of hunting disturbance on waterbirds in Europe: implications for refuge design. Journal of Applied Ecology 34, 1-13. Féret, M., Gauthier, G., Bechet, A., Giroux, J.F. & Hobson, K.A. (2003) Effect of a spring hunt on nutrient storage by greater snow geese in southern Québec. Journal of Wildlife Management 67 (4), 796-807. 158 Capítulo 5 Gill, J.A., Norris, K. & Sutherland, W.J. (2001) Why behavioural responses may not reflect the population consequences of human disturbance. Biological Conservation 97 (2), 265-268. Gillings, S., Fuller, R.J. & Sutherland, W.J. (2005) Diurnal studies do not predict nocturnal habitat choice and site selection of European Golden-Plovers (Pluvialis apricaria) and Northern Lapwings (Vanellus vanellus). The Auk 122 (4), 1249-1260. González, L.M., Arroyo, B.E., Margalida, A., Sánchez, R. & Oria, J. (2007) Can buffer zones have detrimental effects on the conservation of Spanish imperial eagles?: a response from Gonález et al. Animal Conservation 10, 295-296. Goriup, P. (1994) Little Bustard Tetrax tetrax. In: Birds in Europe: Their Conservation Status. Tucker, G.M., Heath, M.F. (eds.). Birdlife International, Cambridge, pp. 236-237. Guillemain, M., Blanc, R., Lucas, C. & Lepley, M. (2007) Ecotourism disturbance to wildfowl in protected areas: historical, empirical and experimental approaches in the Camargue, Southern France. Biodiversity and Conservation 16: 3633-3651. Holmes, N.D., Giese, M., Achurch, H., Robinson, S. & Kriwoken, L.K. (2006) Behaviour and breeding success of gentoo penguins Pygoscelis papua in areas of low and high human activity. Polar Biology 29 (5), 399-412. Howard, N. & Carroll, J. (2001) Driven game shooting on farms in Essex, UK: Implications of land management and conservation. Game & Wildlife Science 18 (2), 157-169. Jarvis, P.J. (2005) Reaction of animals to human disturbance, with particular reference to flight initiation distance. Recent research developments in ecology 3, 1-20. Jolivet, C., Bretagnolle, V., Bizet, D. & Wolff, A. (2007) Status of little bustard in France in 2004. Ornithos 14 (2), 80-94. Klaassen, M, Bauer, S., Madsen, J. & Ingunn, T. (2006) Modelling behavioural and fitness consequences of disturbance for geese along their spring flyway. Journal of Applied Ecology 43 (1), 92-100. Lafferty, K.D. (2001) Birds at a Southern California beach: seasonality, habitat use and disturbance by human activity. Biodiversity and Conservation 10 (11), 19491962. Lucio, A.J. & Purroy, F.J. (1992) Caza y conservación en España. Ardeola 39 (2), 8598. McNamara, J.M & Houston, A.I. (1992) Evolutionarily stable levels of vigilance as a function of group size. Animal Behaviour 43, (4): 641-658. 159 Fabián Casas Arenas Tesis Doctoral Madsen, J. & Fox, A.D. (1995) Impacts of hunting disturbance on waterbirds-A review. Wildlife biology 1 (3), 193-207. Madsen, J. (1998a) Experimental refuges for migratory waterfowl in Danish wetlands. I. Baseline assessment of the disturbance effects of recreational activities. Journal of Applied Ecology 35, 386-397. Madsen J. (1998b) Experimental refuges for migratory waterfowl in Danish wetlands. II. Tests of hunting disturbance effects. Journal of Applied Ecology 35, 398-417. Martinetto, K., Cugnasse, J.M. & Gilbert, Y. (1998) Cohabitation between Mediterranean mouflon (Ovis gmelini musimon x Ovis sp.) and tourists in the massif of Caroux-Espinouse (Herault). Gibier Faune Sauvage 15, 905-919. Martínez, J., Viñuela, J. & Villafuerte, R. (2002) Socioeconomic and cultural aspects of gamebird hunting. REGHAB project, European Commission, Bruselas, Bélgica. Morales, M.B., Suárez, F., Garcia, E.L. & de Juana, E. (2002) Movimientos estaciónales e invernada del sisón. Quercus 193, 34-39. Morales, M.B., Bretagnolle, V. & Arroyo, B. (2005) Viability of the endangered little bustard Tetrax tetrax population of western France. Biodiversity and Conservation 14 (13), 3135-3150. Newton, I. (1998) Population limitation in birds. Academic Press, San diego, USA. Pauli, J.N. & Buskirk, S.W. (2007) Risk-disturbance overrides density dependence in a hunted colonial rodent, the black-tailed prairie dog Cynomys ludovicianus. Journal of Applied Ecology 44, 1219-1230 Percival, S.M., Halpin, Y. & Houston, D.C. (1997) Managing the distribution of barnacle geese on Islay, Scotland, through deliberate human disturbance. Biological Conservation 82, 273-277. Redpath, S. (1988) Vigilance levels in preening Dunlin Calidris alpine. Ibis 130, 555557. Riddington, R., Hassall, M., Lane, S.J., Turner, P.A. & Walters, R. (1996) The impact of disturbance on the behaviour and energy budgets of Brent geese Branta b. bernicla. Bird Study 43, 269-279. Robinson, R.A. & Sutherland, W.J. (2002) Post-war changes in arable farming and biodiversity in Great Britain. Journal of Applied Ecology 39, 157–176. Robinson, J.G. & Bennett, E.L. (2004) Having your wildlife and eating it too: an analysis of hunting sustainability across tropical ecosystems. Animal Conservation 7, 397-408. 160 Capítulo 5 Rocamora, G. & Yeatman-Berthelot, D. (1999) Oiseauxmenaces et a surveiller en France. Listes rouges et recherché de priorités. Société d´Études Ornithologiques de France/Ligue pour la Protection des Oiseaux. París. Roth, T.C. & Lima, S.L. (2007) The predatory behavior of wintering Accipiter hawks: temporal patterns in activity of predators and prey. Oecologia 152, 169-178. Stafford, J.D., Horath, M.M., Yetter, A.P., Hine, C.S. & Havera, S.P. (2007) Wetland use by mallards during spring and fall in the Illinois and Central Mississippi River Valleys. Waterbirds 30, 394-402. Stockwell, C.A., Bateman, G.C. & Berger, J. (1991) Conflicts in national parks: a case study of helicopters and bighorn sheep time budgets at the Grand Canyon. Biological Conservation 56, 317-328 Tamisier, A., Bechet, A., Jarry, G., Lefeuvre, J.C. & Le Maho, Y. (2003) Effects of hunting disturbance on waterbirds. A review of literature. Revue d ecologie-la terre et la vie 58 (4), 435-449. Tapper, S. (1999) A Question of Balance. The Game Conservancy Trust, Fordingbridge, Hampshire. Thiel, D., Ménoni, E., Brenot, J.F. & Jenni, L. (2007) Effects of recreation and hunting on flushing distance of Capercaillie. Journal of Wildlife Management 71, 17841792. Thiollay, J.M. (2007) Effects of hunting on guianan forest game birds. Biodiversity and Conservation 14, 1121-1135. Treves, A. (2000) Theory and method in studies of vigilance and aggregation. Animal Behaviour 60, 711-722. Trouvilliez, J. (1997) Twenty years of hunting reserves and sanctuaries in France: Conclusions and Recommendations. Gibier Faune Sauvage 14 (2), 227-235. Tucker, G.M. & Heath, M.F. (1994) Birds in Europe: their conservation status. Birdlife International, Cambridge. Webb, N.V. & Blumstein, D.T. (2005) Variation in human disturbance differentially affects predation risk assessment in Western Gulls. Condor 107 (1), 178-181. Wolff, A., Paul, J.P., Martin, J.L. & Bretagnolle, V. (2001) The benefits of extensive agriculture to birds: the case of the little bustard. Journal of Applied Ecology 38, 963-975. 161 . SÍNTESIS . . Parámetros reproductivos: Nuevos resultados Antes de desarrollar cualquier tipo de estrategia de gestión para una determinada especie. 1993). en consecuencia. por primera vez. especialmente en aquel hábitat donde la perdiz roja alcanza sus mayores densidades. pretendiendo trazar unas futuras líneas de actuación en las que tanto el aprovechamiento cinegético como agrícola sean compatibles con la conservación del medio y. estas estrategias deberían garantizar la estabilidad de las poblaciones silvestres de perdiz roja. lejos de constituir una actividad necesaria para la supervivencia. se precisa información detallada durante varios años. así como cuales pueden ser las mejores estrategias de gestión agrícola y cinegética. la pseudoestepa agraria (Blanco-Aguiar et al. tanto de la caza propiamente dicha. Uno de los resultados más relevantes de este trabajo es haber constatado el importante papel de los machos en la reproducción de esta especie. y por otro. Rueda et al. como de algunas de las herramientas de gestión más utilizadas en los últimos años (suelta de perdices de granja). sigue siendo sin embargo una de las actividades lúdicas que mayor interés despierta. Por un lado. Para ello. 2003). En el capítulo 1 de esta tesis doctoral se muestra. La caza en España. junto con los efectos indirectos derivados. tanto desde el punto de vista económico como social. como paso inicial es primordial conocer a fondo la ecología reproductiva de esa especie. dada la conocida variabilidad interanual en la cría de la perdiz roja (Lucio 1990. Esta tesis ha tratado de avanzar en ese sentido. Por tanto. en realidad su contribución a la 165 .Síntesis SÍNTESIS: PERSPECTIVAS DE INVESTIGACIÓN FUTURA Y APLICACIONES DE GESTIÓN. la conservación de su hábitat. Al igual que para otras especies. el porcentaje de machos dentro de una población que pueden hacerse cargo del cuidado de una puesta. son un paso clave para desarrollar estrategias de gestión efectivas. Aunque el hecho de que los machos incuben pudiera parecer un comportamiento anecdótico con interesantes connotaciones evolutivas discutidas en dicho capítulo. es importante conocer cuales son los principales puntos donde uno debe incidir. de las especies que lo habitan. lo cual puede beneficiar a otras especies con las que ésta comparte el espacio. conocer los factores que pueden influir en la dinámica poblacional de la principal ave de interés cinegético de la península Ibérica. En ese caso. 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. el clima y la disponibilidad de recursos del medio. 2000). serían necesarias series más largas. Por un lado. como factor de especial importancia sobre los parámetros reproductivos (fecha de inicio de puesta. Así pues. la capacidad de las hembras para la producción de huevos depende de los recursos del medio (Monaghan & Nager 1997. La regulación del tamaño de puesta. Lepage & Lloyd 2004) y está sujeta a fuertes variaciones interanuales (Cattadori et al. A nivel de gestión. Sin embargo. en particular. protocolos experimentales. Watson et al. Villanúa 2007). 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. frecuencia de dobles puestas y tamaño de puesta). la densidad o los depredadores sobre la inversión de los machos en la incubación. puede ser muy útil disponer de este tipo de información. entre los que destacan el compromiso reproductivo de su pareja. Aunque nuestro trabajo ya recoge datos de una cantidad considerable de años. La integración de toda esta información permitiría desarrollar modelos demográficos para predecir las tendencias poblacionales en diferentes circunstancias. poco puede hacerse ante la variabilidad climática 166 . Nuestros datos apuntan al clima. recogiendo información de las diferentes fases del ciclo de vida de la especie. La hembra puede regular su inversión reproductiva en base a diferentes parámetros. tal y como sugieren otros trabajos (Lucio 1990. 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. faltaría explorar en mayor profundidad el papel de la densidad de población y el riesgo de depredación. 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.Fabián Casas Arenas Tesis Doctoral productividad de una población de perdices puede ser importante. que es otra de las piezas fundamentales para completar la información necesaria para el desarrollo de modelos demográficos. para esclarecer cual es la importancia relativa del clima. 1999. Otros factores como la edad y la condición física y. la densidad de población también pueden contribuir a explicar la frecuencia de aparición de este comportamiento. 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. o muestreos simultáneos en diversas áreas de estudio. Fernández & Reboreda 2007). 2003). en prácticamente toda su área de distribución. que la alimentación suplementaria de perdices silvestres puede tener serias consecuencias negativas sobre su fisiología y anatomía interna. Esta modalidad puede a su vez formar parte integral de la gestión cinegética. Diversas razones podrían explicar este 167 . el aporte suplementario de alimento no fue una de las herramientas de gestión utilizada. y como señalamos en la Introducción de esta tesis. En tales casos. sino igualmente en la supervivencia y condición física de la perdiz roja. como de hecho es frecuente. Urge profundizar en este tipo de aspectos en relación con la caza de la perdiz con reclamo. que se creé destruyen nidos de otras perdices). Pero. 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”. los machos abatidos mediante esta modalidad podrían ser aquellos más agresivos. y por tanto la caza con reclamo no tendría un gran efecto sobre la población. es una herramienta de gestión frecuente (Díaz 2006). la caza con reclamo se usa como herramienta para reducir el número de machos. Por tanto. es la caza de perdiz con reclamo. que posiblemente tengan menor tendencia a incubar puestas (Mougeot et al. serían necesarias futuras investigaciones para clarificar los efectos del aporte suplementario de alimento. por otro lado. Sin embargo. las poblaciones naturales de perdiz roja sufrieron una marcada regresión en las últimas décadas. no solo en la ecología reproductiva. A la luz de nuestros resultados. que pueden conducir a problemas de supervivencia en libertad (Millán et al. ya que pueden ser clave para mejorar la estrategia de gestión de sus poblaciones. Sí se conoce sin embargo. datos no publicados). Por otro lado. pero sí se podría actuar para reducir dicha variabilidad interanual en la disponibilidad de recursos tróficos en el período más crítico de la reproducción. ¿Gestión del hábitat o control de depredadores? Como se comentaba en la Introducción de esta tesis doctoral. Dentro de nuestra área de estudio. una modalidad de aprovechamiento cinegético complementario tras el cierre de la veda general en muchos cotos. 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. aunque se sabe muy poco sobre su efecto en los parámetros reproductivos de la perdiz roja en el área mediterránea.Síntesis interanual experimentada en ambientes mediterráneos (Blondel & Aronson 1999). 2003). Duarte & Vargas 2002). De la Concha et al. Castaño 1995. 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). 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. Lucio & Purroy 1992. no sólo beneficiarían a las poblaciones de perdiz. en lo posible. 2006) y las que pueden ser potencialmente afectadas por la cosecha. La selección positiva de las lindes como sustrato de nidificación. particularmente en los medios agrarios (Lucio & Purroy 1992. la actuación sobre la 168 . el control de depredadores es la herramienta de gestión más utilizada (Arroyo & Beja 2002). especialmente en áreas agrarias. junto al efecto relativamente más débil de la depredación. Arroyo et al. 2002) o los sisones (Tetrax tetrax. Blanco-Aguiar et al. 1998.b. 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. Fuller 2000). Carole Attié. 2004. comunicación personal). junto con el mayor éxito de nidificación de los nidos situados en estos hábitats. sino también a un gran número de especies que comparten su hábitat. Estas medidas principales serían el mantenimiento y. nuestros resultados indican que al menos en lo que se refiere a la fase de puesta e incubación. Vickery et al. Estas acciones. Blanco-Aguiar 2007). Sin embargo.Fabián Casas Arenas Tesis Doctoral declive. que la principal estrategia de gestión para el mantenimiento de poblaciones silvestres saludables es la gestión del hábitat (Rands 1987a. como los aguiluchos (Circus sp. especialmente aquellas afectadas por la disminución de la superficie de las lindes (Tella et al. Vargas et al. 2003. el fuerte efecto de la cosecha sobre el éxito de nidificación de la perdiz. la desaparición de las lindes como consecuencia de la intensificación agrícola (Pain & Pienkowski 1997. 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). Blanco-Aguiar et al. pueden ser los dos factores directos más importantes para explicar el declive generalizado de las poblaciones de perdiz roja. unidas a la preservación del tradicional paisaje en mosaico de los campos de cultivo. 2002. Por otro lado. pero la más importante parece ser la alteración del hábitat. evidencian una vez más.. Nuestros resultados permiten acotar cuáles serían las estrategias aplicables más importantes en cuanto a gestión agraria. 2006. Sin embargo. Según nuestros resultados. Peiró 1992. Por ello. junto al impacto negativo de las prácticas agrícolas (principalmente cosecha) sobre el éxito de nidificación. 2001. se han ido acumulando evidencias de los efectos negativos de estas sueltas. sin tener en cuenta que las temporadas de caza venideras dependen de los individuos que se dejen vivos para la siguiente temporada de cría. y por tanto. Gortazar et al.Síntesis gestión agraria sería una estrategia mucho más eficaz que el control de depredadores. Por un lado. 2005). tanto sobre otras especies con las que comparten el mismo hábitat como sobre las poblaciones silvestres de las propias especies liberadas (Tompkins et al. Pero. Es importante reseñar que esta baja importancia relativa de la depredación no parece deberse a la gestión relacionada con el control de depredadores. ya que su período de permanencia en el campo es relativamente bajo. La sobrecaza no es sólo un efecto derivado de la sueltas de aves procedentes de granja. los efectos tanto en las propias poblaciones de perdices como en las poblaciones de otras especies que habitan en la misma área. la baja efectividad de las sueltas de aves procedentes de granjas ha sido demostrada en varias especies (Leif 1994. 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. sino que puede producirse en cualquier área donde que no marque un cupo de capturas. también podrían ser distintos. los considerados más dañinos para la perdiz roja. y en alguno de ellos la abundancia de depredadores antropófilos (gatos y perros asilvestrados). 2007). De hecho. tanto a nivel nacional como internacional. 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. lo cual podría dar lugar a pensar que el riesgo potencial (transmisión de parásitos e introgresión genética) sería muy reducido. en prensa) y la introgresión genética (Blanco-Aguiar 2007). independientemente 169 . 2000. la transmisión de parásitos (Villanúa et al. al menos en nuestra área de estudio. principalmente debido a la sobrecaza (Keane et al. por el contrario. A pesar de ello. 2005). Putaala & Hissa 2003). 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. Villanúa et al. hay notables diferencias en la intensidad del control de depredadores entre los cotos estudiados. es relativamente alta. y en poco más de 3 años de protección la densidad de las perdices se vio triplicada (Martínez et al. a pesar de esa sensibilidad a la sobreexplotación. también puede suponer una amenaza para la conservación de la biodiversidad (Tompkins et al. La perdiz roja es una especie muy sensible a la sobreexplotación cinegética.Fabián Casas Arenas Tesis Doctoral de que se suelte perdiz o no. 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. Durante nuestro período de estudio. la caza intensiva ha podido contribuir a la extinción local de la amenazada perdiz pardilla Perdix perdix (Watson et al. A pesar de que la sobreexplotación cinegética podría estar especialmente ligada a ésta práctica de gestión. en prensa). Otro de los riesgos potenciales de las sueltas. en los que tienden a producirse con mayor probabilidad sobreexplotaciones. Villanúa et al. nos encontramos otros casos que mantienen la gestión durante todo el año. este grave problema de sobreexplotación sólo fue observado en el coto donde la suelta de perdices era la base de la gestión. 2002). se ha constatado igualmente tanto el riesgo de transmisión interespecífico 170 . Aunque esta última especie es considerada de interés cinegético. Por otro lado. En nuestra área de estudio. como es la transmisión intra. en 1996 el 30 % del país estaba acotado. Por tanto. agua y alimento suplementario). A pesar de esto. en el Reino Unido por ejemplo. las poblaciones de perdiz tienen gran capacidad de recuperación. esto no ocurre siempre. la sobrecaza afecta a la viabilidad poblacional de muchas otras galliformes (Keane et al. quizás el mejor ejemplo es el desastre portugués durante la conocida como revolución de los claveles (1974-1988). 2007). 2007). Durante ese período se esquilmaron las poblaciones de perdices. 2005).e inter-especifica de parásitos intestinales. En tales enclaves la presencia de la perdiz esta íntimamente vinculada a las sueltas con aves procedentes de granjas. puesto que la caza era libre y la única limitación era un cupo de piezas por día (Martínez et al. En cuanto a la sobrecaza debido a las sueltas masivas de perdices rojas. 2002). y de poco o nada sirve una gestión adecuada del hábitat. 2001. sus poblaciones han sufrido un gran declive hasta el punto que su caza tradicional a dejado de ser sostenible (Aebischer 1997). 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. y de las propias poblaciones silvestres de perdiz (Villanúa et al. tras la aparición de la Ley de 1988 (promoción de acotados y caza sostenible). De forma más general. urge una investigación detallada sobre los efectos de los parásitos sobre variables como la condición física. Por otro lado. hemos detectado que la malaria puede invadir de forma explosiva las poblaciones de perdices de granja (García et al. ya que la diseminación de las enfermedades causadas por estos protozoos (géneros Plasmodium. paralelamente. 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. Perez et al. Villanúa 2007). y muy superiores a las encontradas recientemente en un ave que comparte hábitat con las perdices. o la supervivencia. la ausencia de información en lo que a parásitos sanguíneos se refiere. Nuestros resultados son 171 . En primer lugar. especialmente en áreas donde se han soltados perdices con fines cinegéticos (Blanco-Aguiar 2007). 2007). Haemoproteus o Leucocytozoon) puede tener importantes consecuencias en la dinámica poblacional de las aves (Valkiūnas 1993. Merino et al. el éxito reproductor. encontramos unas prevalencias de parásitos sanguíneos muy altas para aves de estos ambientes. y tal y como adelantábamos en la Introducción. como intraespecífico de parásitos intestinales (Villanúa et al. la inversión en cuidados parentales. Puesto que. 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). datos no publicados). Finalmente. A pesar del cada vez más amplio conocimiento sobre las diferencias entre las comunidades de parásitos de aves de granja y silvestres (Millán 2004. Dados los hallazgos comentados anteriormente. 2007). es conocido que las perdices de granja pueden llegar a sobrevivir y criar en el campo (Duarte & Vargas 2004). poco se sabe acerca del papel de estos parásitos sobre la eficacia biológica de las perdices (Blanco-Aguiar 2007). Para ello el desarrollo de estudios experimentales sería de gran ayuda. en una zona de estudio cercana y usando una metodología similar (Ortego et al. además. es posible que las prevalencias anormalmente altas de las perdices sean otro efecto negativo no deseado de las sueltas de aves de granja. dejaba vacío un campo de investigación que precisaba de un análisis detallado. 2000. en prensa). Encontramos.Síntesis (Villanúa et al. 2000). lo que vendría a sugerir que la suelta de perdices puede estar introduciendo linajes de parásitos sanguíneos nuevos en las poblaciones silvestres. A pesar de la reducida eficacia de las sueltas (Gortázar et al. 2004). 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. se hablaba con libertad sobre la existencia en las granjas de perdices que procedían de cruces sucesivos entre A. y en un año tan reciente como 1992. Cuando se comenzó a usar este sistema de gestión no parecía haber demasiada preocupación sobre lo que se estaba soltando al campo. se ha comprobado que la gestión sanitaria es prácticamente inexistente cuando no completamente desconocida (Martínez-Lorca 2002). los híbridos tenderían a desaparecer de las poblaciones. como el éxito de emparejamiento o la supervivencia de pollos de perdices híbridas. Esta información sería importante para desarrollar una estrategia de gestión efectiva para conservar la pureza genética de la perdiz roja silvestre. rufa x A. En cualquier caso. en parte no está en las propias sueltas si no en el estado sanitario y genético de las aves procedentes de las granjas. incluso una vez superado el período crítico de las primeras semanas después de la suelta.Fabián Casas Arenas Tesis Doctoral los primeros que aportan datos sobre la reproducción de estas perdices híbridas en el medio natural. como parecen indicar nuestros resultados. En cuanto al estado sanitario. que el éxito reproductivo de las perdices híbridas en libertad podría ser mayor. Otra explicación alternativa sería la asociación entre algunos parásitos y variables fisiológicas. Sólo muy recientemente ha comenzado a surgir una cierta preocupación sobre la calidad genética y sanitaria de las perdices de suelta. 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. que podrían ser un indicativo de posible pérdida de adaptación local de las perdices híbridas frente a los parásitos locales (Blanco-Aguiar 2007). graeca (Nadal 1992). 172 . y los machos híbridos. chukar o A. Estos resultados indican. por tanto. Un resultado importante es la más baja supervivencia detectada en individuos híbridos. mayor tendencia a incubar. en un estudio realizado recientemente en las granjas de perdices de la provincia de Ciudad Real. rufa x A. 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. Sin embargo. siendo urgente aplicar los métodos de detección de híbridos y de gestión sanitaria para mejorar la calidad de los ejemplares que están siendo liberados. este resultado sugiere que. En general. en el que es bien conocida la alta mortalidad que sufren (Gortázar 1998). Se necesitaría más información sobre aspectos no abarcados hasta el momento. a largo plazo. el origen de la amenaza que ahora nos encontramos en el campo. también encontramos que las perdices híbridas tienen mayores tamaños de puesta. Thiel et al. 2002). Klaassen et al. Sin embargo. nuestros resultados indican que en el campo las perdices híbridas podrían ser incluso más productivas que las rojas. no existe ningún trabajo realizado en áreas agrícolas sobre el efecto de la caza en el comportamiento de las aves. 2007. 2006. a la espera de información más detallada que permita desarrollar modelos demográficos. 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. que aportan resultados reveladores sobre el efecto de la caza en el comportamiento y distribución de distintas especies (Madsen & Fox 1995. Sin embargo. donde está muy extendido el uso de reservas de caza dentro de los cotos. Podría pensarse que la solución a este problema. se desarrolló en Francia. Durante la práctica de esta actividad de alto impacto. y por tanto. son muchas las especies que pueden verse directa o indirectamente implicadas. pero también en otros hábitats. la solución podría estar en la misma técnica que creó el problema: sueltas con perdices de buena calidad genética. a pesar de que en estos hábitats la caza es un aprovechamiento alternativo al uso de la tierra muy extendido (Bernabeu 2000. 2005. Duriez et al. ya que los genotipos híbridos podrían estar extendiéndose en las poblaciones incluso sin recibir refuerzos adicionales de perdices de suelta. Thiollay 2007). asociadas a caza intensiva.Síntesis Las administraciones han comenzado también a tomar cartas en el asunto. hasta donde sabemos. 173 . Por el contrario. 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. no consideraríamos aconsejable eliminar completamente las sueltas. y así se reclama desde los sectores más extremistas. Existen numerosos estudios realizados principalmente en ambientes acuáticos. aunque de forma mucho más tímida y lenta de lo deseable. estrategia que contribuiría a revertir la estructura genética de las poblaciones. sería prohibir esta técnica de gestión. Martínez et al. El trabajo presentado en el capítulo 5 de esta tesis doctoral. Fox & Madsen 1997. Howard & Carroll 2001. En estas reservas distintas especies podrían encontrar refugio porque no está permitido cazar. y apoyándonos en la nueva Ley de Patrimonio Natural y Biodiversidad. la ganga ortega (Pterocles orientalis) y la avutarda (Otis tarda). A pesar de ello.Fabián Casas Arenas Tesis Doctoral Nuestros resultados mostraron que en las tres especies estudiadas (sisones. estas zonas suelen situarse en áreas de menor valor faunístico. Teniendo en cuenta la importancia socioeconómica y las particularidades ecológicas de esta especie. gestión agrícola y gestión cinegética Para integrar conjuntamente el aprovechamiento cinegético y agrícola. La normativa vigente a nivel estatal. la perdiz 174 . Si bien aunque se cumple la normativa. Además. estos resultados podrían ser igualmente extrapolables a zonas agrícolas del centro peninsular. En nuestro caso. A su vez. que puedan beneficiar tanto a especies cinegéticas como a otras presentes en los mismos hábitats. En concreto para Castilla-La Mancha. 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. los resultados sugieren que la caza puede ser un estímulo adicional que desencadene la migración en los sisones. deberán reservar del ejercicio de la caza al menos un 10 % de la superficie total del coto. actuando como refugio eficaz en los días que se desarrollaba dicha actividad. sería importante desarrollar este tipo de trabajos en zonas del centro peninsular. sería un importante paso previo a la creación de una red de refugios para establecer una pautas generales de gestión. donde están presentes las tres especies estudiadas junto a otras como la ganga ibérica (Pterocles alchata). EPÍLOGO: Integración de conservación. sólo aquellos terrenos cuya superficie sea igual o superior a 500 hectáreas. añadiendo otras especies de gran interés de conservación e incluyendo a las especies objeto de caza. hemos basado la estrategia en estudiar los principales factores que pueden afectar a la viabilidad poblacional de la perdiz roja. También comprobamos que las reservas de caza cumplían una función importante. avefrías y chorlitos dorados) la actividad cinegética inducía cambios de comportamiento que podrían suponer mayores gastos energéticos. Aunque en España existe la figura de las reservas de caza dentro de cada acotado. junto a la conservación de la biodiversidad. comprobar la utilidad de las reservas de caza fuera del período hábil (éxito de reproducción y mortalidad dentro y fuera de las reservas). Aunque este trabajo se realizó en el centro oeste de Francia. 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. no son lo suficientemente eficientes como para evitar la introducción de nuevos parásitos en el campo (Villanúa et al. en particular barbechos. quizás el principal riesgo no estribe en la suelta de perdices per se.Síntesis roja puede llegar a desempeñar la función de especie “paraguas” (al igual que sucede con muchas otras especies cinegéticas) dentro del ecosistema. Mejora en la normativa sanitaria y exigencia de aplicación de programas de gestión sanitaria. y en consecuencia. Mantenimiento del mosaico paisajístico característico de las áreas agrícolas. 2007b). podemos establecer una serie de medidas que podrían adoptarse en beneficio mutuo. mediante controles genéticos de las granjas de producción. Por lo que respecta a la gestión del hábitat (agrícola). 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. 175 . puedan resultar beneficiosas o no para otras especies que comparten su territorio. sino en el origen genético y control sanitario de las aves en las granjas previamente a la suelta. para conseguir estos objetivos se debería mejorar la aplicación de la normativa de ecocondicionalidad de la PAC. En el caso de los problemas derivados de las sueltas. principalmente: Incremento y/o mantenimiento de las lindes y fomento de medios de cría alternativos al cereal. que muchas de las acciones encaminadas a mejorar el rendimiento y conservación de sus poblaciones. Hasta el momento los protocolos de control sanitario adoptados. Retraso de las fecha de cosecha. como de las poblaciones de aves esteparias amenazadas. Por ello. 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. según los resultados presentados en esta tesis doctoral. al menos en las bandas externas de las parcelas de cultivo. En particular. tanto de las poblaciones de perdiz roja. y la transmisión de parásitos. como son la introgresión genética. pp. 208-209. R. B. Universidad de Castilla-La Mancha. Del Moral). & Bretagnolle V. T & A. Reino Unido. Blondel.L.A. N. Madroño. Arroyo. R. Virgós. 212-213.C. Hagemeijer & M. Virgós. & Beja. & Aronson. pp. Bernabeu. Tesis doctoral. 182-185.Fabián Casas Arenas Tesis Doctoral - Detección de áreas críticas para la conservación de la pureza genética de la perdiz roja silvestre. Report WP2 to REGHAB project. A. & Villafuerte. (1997) Red-legged Partridge Alectoris rufa. C.es/irec/reghab/ informes. (2007) Variación espacial en la biología de la perdiz roja (Alectoris rufa): una aproximación multidisciplinar. A. Tesis Doctoral. R. Madrid. (2004) Perdiz Roja (Alectoris rufa). Bruselas. - Marcaje estable (anilla metálica) de todas las aves liberadas de granja. España. en las que se debe impedir la llegada de híbridos procedentes de sueltas. (2002) Conservation of the Montagu's harrier (Circus pygargus) in agricultural areas. Blanco-Aguiar.J. J. España. Blanco-Aguiar.htm) European Commision. Atlas de las aves reproductoras de España. Martí & J. (2003) Perdiz Roja (Alectoris rufa).. P. España. para su posterior control y seguimiento. BIBLIOGRAFÍA Aebischer. Madrid. & Villafuerte.J. Londres. Atienza).. el establecimiento de una red de reservas enclavadas en zonas de gran riqueza faunística. E. Oxford.J. en lugar de situarla en zonas marginales que realmente no tienen ningún efecto sobre las poblaciones de aves. R. En: The EBCC Atlas of European Breeding Birds: Their Distribution and Abundance. Por último. Libro Rojo de las Aves de España. 176 . Garcia J. J. D. Universidad Complutense de Madrid. pp.M. Arroyo. (eds. podría ser una medida mucho más efectiva que la actual distribución de áreas de reserva. Blanco-Aguiar. González & J. España. Poyser. E. (http://www. Dirección General para la Biodiversidad-SEO/BirdLife. J.C. Animal Conservation 5.. & Lucio. (1999) Biology and wildlife of the Mediterranean region. Dirección General de Conservación de la Naturaleza y Sociedad Española de Ornitología. (eds. J. Blair).A. (2002) Impact of hunting management practices on biodiversity. 283-290. (2000) Evaluación económica de la caza en Castilla-La Mancha. (eds W.. B. J.T.uclm. Oxford University Press.A. . A. pp 119-134.. & Reboreda. (eds. & Vargas. Ecology and Conservation of Lowland Farmland Birds. Madrid. Palencia.. & Ferrand. Evans.M. 215–222. P. 332-346. Journal of Applied Ecology 34. Fernández. & Vargas. Biological Conservation 122. (1995) Efecto de la actividad de siega y causas de fracaso reproductivo en una población de aguilucho cenizo (Circus pygargus) en el SE de Ciudad Real. 167-172. J. (1998) Las repoblaciones con perdiz roja. A. Journal of animal ecology 68. I. S. (2000) Relationship between recent changes in lowland British agriculture and farmland bird populations: an overview.M.. (2006) Medidas beneficiosas para las aves financiables a través del nuevo reglamento de desarrollo rural. R. & Martín. Villafuerte. I. M.J. J. Ibis 126. Grice & J. Ibis 149. FEDENCA. Game and Wildlife Science 21. Madrid. J. pp. Duarte. Fuller. FEDENCE-EEC. Lucio & M. J. J. Barbraud.J. pp. Cattadori. (1984) Double nesting of the red-legged partridge Alectoris rufa. 55-61. Duarte. Sáenz de Buruaga). (1997) Behavioural and distributional effects of hunting disturbance on waterbirds in Europe: implications for refuge design. C.Síntesis Castaño. R.J. España. 540-549. Gortázar. Green. Aebischer. (2002) Los sumideros de perdiz roja a lo largo del ciclo anual. P. Aportaciones a la gestión sostenible de la caza. (2005) Factors affecting population dynamics of Eurasian woodcocks wintering in France: assessing the efficiency of a hunting-free reserve. Merler. J. (2007) Costs of large communal clutches for male and female Greater Rheas Rhea Americana. O. N. C. 5-16. Sugerencias para su diseño y aplicación en NATURA 2000. J. 1-13. A. R. De la Concha.P. En: La perdiz roja. Madrid. (1999) Synchrony. Proyecto fin de carrera de Ingeniería de Montes de la Universidad de Valladolid. S. British Ornithologists' Union. Vickery). 23-30. Gortázar. (eds. C. Hernández. (2000) Success of traditional restocking of red-legged partridge for hunting purposes in areas of low density of northeast Spain Aragón. (2004) Field interbreeding of released farm-reared Redlegged partridges (Alectoris rufa) with wild ones. Duriez. SEO/BirdLife..E.V. C. Ardeola 42. Hudson. Fox. scale and temporal dynamics of rock partridge (Alectoris graeca saxatilis) populations in the Dolomites. & Madsen J.C.D. 89-97.A. 101-126. Y. Díaz. 177 .. & Pinilla. & Rizzoli A. C.D. Zeitschrift fur Jagdwissenschaft 46.M. Eraud. (2006) Caracterización de la gestión cinegética y agraria en cotos de caza menor de la Comarca de Montiel (Albacete) y evaluación de su influencia en las capturas de perdiz roja (Alectoris rufa). Tring.J. G. . Quails and Francolins. Proceedings of the royal society of London Series b: biological sciences 267. Journal of Wildlife Management 58 (3). (2006) Modelling behavioural and fitness consequences of disturbance for geese along their spring flyway. R. Gortazar. Wildlife biology 1 (3). Influencia de las condiciones climáticas en la productividad de la perdiz roja (Alectoris rufa). Bauer. UK: Implications of land management and conservation. Leif. (2005) Correlates of extinction risk and hunting pressure in gamebirds (Galliformes). & Fox. 270-273. 2507-2510. Trabajo de fin de Master. & Arriero. 216– 233. (2002). & Nager. J. Bruselas. F. & Lloyd P. Bélgica. (eds. P. (2001) Driven game shooting on farms in Essex. T. España. Estudio descriptivo de las granjas de perdices de la provincia de Ciudad Real. Lucio. Journal of Applied Ecology 43 (1). Millán. Symp. P. A. de L. IREC. (2004) Avian clutch size in relation to rainfall seasonality and stochasticity along an aridity gradient across South Africa. (1995) Impacts of hunting disturbance on waterbirds-A review. R. J. J. Sanz. (1994) Survival and Reproduction of Wild and Pen-Reared Ring-Necked Pheasant Hens. 229-233. N. Birkan.J. 501-506. 207-218. E. C. Game & Wildlife Science 18 (2).J. R.D.Fabián Casas Arenas Tesis Doctoral Howard. J. Klaassen. M. Monaghan. Ciudad Real. A. 178 . S.J. Universidad de Zaragoza. J. M. J. & Purroy. G.. Tesis Doctoral. & Villafuerte. Gibier Faune Sauvage 9. Aebisher & S. Lepage. (2004) Alteraciones asociadas a la cría en cautividad de Galliformes silvestres. 259268. 92-100. Millán. (2003) Does supplementary feeding affect organ and gut size of wild red-legged partridges Alectoris rufa? Wildlife Biology 9 (3). A. Biological Conservation 126.R. & Ingunn.K.. 417-430. Lucio. N. Brooke. Keane. Martínez Lorca. & Villafuerte. Madsen. & Carroll. F. S Madsen. A.J. J. J. (1992) Red-legged partridge (Alectoris rufa) habitat selection in Northwest Spain. (2002) Socioeconomic and cultural aspects of gamebird hunting. J. Dowell) First Intern. D. (1997) Why don’t birds lay more eggs? Trends in Ecology and Evolution 12. Merino. European Commission. 157-169.P.J. Viñuela. Potts. Ostrich 75 (4). REGHAB project. & Mcgowan. on Partridges.J. (2000) Are avian blood parasites pathogenic in the wild? A medication experiment in blue tits (Parus caeruleus).. J. M. 1990. 193-207. A.G.D. Ardeola 37 (2). Moreno. Martínez. (2004) Use of radiotracking techniques to study a summer repopulation with red-legged partridge (Alectoris rufa) chicks. R. J. J. C. (2007) Genetic characterization of avian malaria (Protozoa) in the endangered lesser kestrel Falco naumanni. & Hissa. España. Universidad de Alicante. 882-888.R. 137-145. Rueda. Journal of Wildlife Management 71. pp. Poultry Science 83. 479-87. Cordero. Londres. 87-100. (1998) Conflicts between lesser kestrel conservation and European agricultural policy as identified by habitat use analysis. Fundación La Caixa. G.. La perdiz roja. Rands.. V. (1986) Effect of Hedgerow Characteristics on Partridge Breeding Densities. AedosFundación “La Caixa”. 407-418. F. Rands. & Notario. M. Barcelona. caza y vida silvestre. (1992) Ecología de las poblaciones de perdiz roja (Alectoris rufa) en la provincia de Alicante y su aplicación a la gestión cinegética. & Jenni. D. M.. P. A.R. 1153-1156. (1987b) Recruitment of grey and red-legged partridges (Perdix perdix and Alectoris rufa) in relation to population density and habitat. & Donazár. 1992.M.G. D. Hiraldo. & Pienkowski. Conservation biology 12. 2-9.Síntesis Nadal. Nadal.. Gestión del Hábitat. Putaala. M. M. M. Bulletin Mensual Office Nacional de la Chasse 184. Thiel. Olmedo. J. Journal of Applied Ecology 23. 179 . Tesis doctoral. España.W. Rands. Díez..R..R. Alonso.W.A..J.J. (2007) Effects of recreation and hunting on flushing distance of Capercaillie. Brenot. (eds.E. Forero.R. Academic Press. L. Calabuig. 593-604.. J. 17841792...W. Tella. (2003) Breeding dispersal and demography of wild anda handreared grey partridges Perdix perdix in Finland. & Comalrena. & Bartolomé. Peiró. The Common Agricultural Policy and its implications for bird conservation. V.W.A. Pain D. (1987a) Hedgerow management for the conservation of partridges Perdix perdix and Alectoris rufa. Ortego. Reino Unido. Biological Conservation 40. Baragaño. 127-139. Parasitology Research 101. J. Barcelona. España. Ménoni. M.F. Wildlife Biology 4. M. Pérez. P. & Aparicio. J.A. J. J. E. Problemática de las poblaciones de perdiz roja. Gaudioso. bases ecoetológicas para tener éxito con las repoblaciones.) (1994) Predación.L. A.J. (1997) Farming and birds in Europe. J.. J. Journal of Zoology 212. (1993) Nidification de la perdrix rouge (Alectoris rufa) dans la région de La Mancha (Espagne). .. Valkiūnas. P. European Journal of Wildlife Research 52. 2126-2136. J. & Fuller. & Gortázar.. Carter. E.. Greenman. J. 1121-1135. Vickery. J.M. Morales. J. (2006) Land use and environmental factors affecting red-legged partridge (Alectoris rufa) hunting yields in southern Spain.. Viñuela.. F. Pérez-Rodríguez. Kenward. Casas. Arroyo. J. N. DOI 10. España. J. Universidad de Castilla La Mancha. Hudson.. D. (2000) Wheather and synchrony in 10-year population cycles of rock ptarmigan and de red grouse in Scotland.. Barbosa... D. S. Ecosystem & Environment 89..A.. (2002) The potential value of managed cereal field margins as foraging habitats for farmland birds in the UK. R. A. Biological Reviews 80. (2005) Birds of prey as limiting factors of gamebird populations in Europe: a review.J. C.. Viñuela. 188-195..L.. European Journal of Wildlife Research. Villanúa. Ecology 81 (8).J. B. D..M. P. Alzaga. 171-203... M. & Viñuela.. (2007b) How effective is pre-release nematode control in farm reared red-legged partridges (Alectoris rufa)? Journal of Helmithology 81. R. Parasitology 122. Villanúa. J. (2007) Parásitos de la perdiz roja (Alectoris rufa): implicaciones para su aprovechamiento cinegético y conservación. Ibis 149.V. Thirgood. F. Watson.B. Gortázar. (2001) Differential impact of shared nematode parasite on two gamebird hosts: implications for apparent competition. & Rothery. Beja. V. R. S. Korpimäki. 47-60. Acevedo. Rodríguez. & Real. Farfán. C. Agriculture. Viñuela.M. A negative effect of red-legged partridge Alectoris rufa releases on steppe bird conservation?.. Guerrero. O.101-103 Villanúa. R. M. Valkama.. Pérez-Rodríguez.. Tompkins. & Gortazar. Villanúa. L. García de la Morena. G. P. Bro. E. Biodiversity and Conservation 14. Ekologija 1.. J.. 405-406.M. D. E. A. (1993) Pathogenic influence of haemosporidians and trypanosomes on wild birds in the field conditions: facts and hypotheses. Tesis Doctoral. D. Moss. Vargas.1007/s10344-007-0130-2.. M. J. Casas. (2007a) First occurence of Eucoleus contortus in a little bustard Tetrax tetrax. (en prensa) Sanitary risks of red-legged partridge releases: introduction of parasites. Bretagnolle. S. Redpath. J. C. L. 41-52. Mañosa. V.. P. 180 .C.Fabián Casas Arenas Tesis Doctoral Thiollay. 187-193... (2007) Effects of hunting on guianan forest game birds. CONCLUSIONES . . Controlar la introgresión de genomas alóctonos es una pieza de vital importancia para la conservación a largo plazo de esta especie. Particularmente el mantenimiento y creación de lindes. esto podría dar lugar a generar programas de colaboración entre agricultores. cazadores y conservacionistas que beneficiarían a un gran número de especies.La suelta de perdices procedentes de granja supone una amenaza para la integridad genética de la perdiz roja. tasa de incubación de machos. El plan de gestión debería también estar integrado por la creación de una red de refugios a escala internacional.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.Los machos de perdiz roja juegan un importante papel en el éxito reproductivo. 3.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. la variabilidad encontrada entre años en tamaños de puesta. La situación podría empeorarse por los mayores tamaños de puesta de las hembras híbridas.El impacto negativo de la cosecha en el éxito reproductivo de la perdiz roja ha sido detectado en otras especies de importancia conservacionista. es esencial para comprender las implicaciones de tales acciones para la conservación de la vida silvestre y el control de enfermedades. apuntan al clima como factor de especial importancia sobre estos parámetros. sería una importante medida para reducir el efecto de la caza sobre esta especie. 6.La perdiz roja es una especie cinegética con alta productividad. Alrededor del 50 % de los machos pueden hacerse cargo de la incubación de un nido. 183 . así como un retraso en la fecha de cosecha. Proponer urgentes programas de gestión que detengan la suelta de perdices híbridas. Por tanto. 5. en este caso la perdiz roja. Estas disposiciones deberían ser consideradas una prioridad entre las medidas de eco-condicionalidad de la PAC. al menos en la franja más externa de las parcelas de cereal. Retrasar la fecha de inicio de la caza en áreas donde existen poblaciones de sisón común migratorias. renovar los pools genéticos en áreas con introgresión genética. aunque el hecho de que los machos incuben pudiera parecer un comportamiento anecdótico carente de importancia. fechas de inicio de puesta y éxito de eclosión. y preservar las poblaciones en buenas condiciones genéticas son medidas imprescindibles para la conservación de esta especie. 2. salvo en años donde la productividad general de la especie es muy bajo. Esta condición debe tenerse en cuenta a la hora de diseñar los planes estratégicos de gestión. 4.Cambios en la gestión agrícola serían más efectivos para mejorar el éxito reproductivo de la perdiz que el control de depredadores en zonas agrícolas.Conclusiones 1. en realidad su contribución a la productividad de una población de perdices es importante. 7. 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. Valorar las consecuencias del manejo humano sobre los hospedadores. 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. 184 . La perturbación asociada a la caza induce cambios de comportamiento que podrían suponer mayores gastos energéticos.Fabián Casas Arenas Tesis Doctoral 8. AGRADECIMIENTOS . . saque una perdiz de una bolsa. afortunadamente cuento con una familia a la que adoro. sería más o menos a la misma vez que aprendí a atarme el cordón de mis zapatillas. afortunadamente no fue mi caso. Después de esa época. pero ése. pero sobre todo por ser los mejores padres y hermana del mundo.Agradecimientos Si no recuerdo mal. Si hay alguien que por encima de todo el mundo merezca mi agradecimiento. fue antes de mi etapa de párvulos cuando comencé a tener claro a que quería dedicarme de mayor. Por otro lado. pero es que sin duda. Gracias. Que un día de lluvia te llegue tu hijo a casa lleno de barro. que siempre han tenido plena confianza en mí y me han apoyado en todo lo que me he propuesto. 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. tanto aficionados como profesionales. en cero con dos te monte en la cochera un laboratorio móvil. En fin. y de mis continuas juergas y viajes (mi segunda ocupación). gracias por vuestro cariño. sino también por participar y disfrutar de ello conmigo. tanto en lo bueno como en lo malo. Es por ello que esta tesis no solo va dedicada a ellos. quizás las ideas de un niño pueden cambiar mucho. siempre presentes. Juntos habéis conseguido que me olvide del resto de menesteres y quehaceres. Ya se sabe. porque no me imagino haciendo otra cosa. el aumento de los niveles de testosterona. Puede que Félix Rodríguez de la Fuente tuviese mucho que ver. Cuantas comidas y cenas rodeado de ellos. estudiar a los pájaros. Valga desde aquí mi agradecimiento a la persona que lanzó a correr el sentimiento latente de mi vocación. y te diga que la sujetes que tiene que sacarle sangre. el descubrimiento de nuevos mundos. Este “bichologo” como me dicen mis titas 187 . no solo por respetar mi decisión de dedicarme a lo que realmente me gusta. Esta frase es muy repetida por muchos de los que amamos esta profesión. y que han estado siempre apoyándome. el lado oscuro de la luna. después se vaya corriendo y te dejé la cochera llena de barro y plumas. Aún hoy día. sigue siendo referente para muchos naturalistas. para que me ocupase única y exclusivamente de la tesis (cuantas veces habré escuchado que vivo en un “hotel”). no basta solo con quererlo para no mandarle más allá de Fernando Po. la adolescencia. Y digo latente. son sin duda mis padres y mi hermana Gema. sino que a pasado a formar parte de ellos. ¿A ver a qué nos dedicamos ahora? Tendré que echarme una novia. porque sentir el apoyo de la familia unida te empuja a lograr tus sueños. que estuve entrenando el primer año de tesis. al resto de mis primos. De lo que son capaces mis directores porque su doctorando se sienta a gusto. Gracias a todos por vuestro cariño y apoyo.Fabián Casas Arenas Tesis Doctoral “las Bartolas” (Estrella. Jesús. porque son muchos momentos vividos junto a ellos. Disculpad si me dejo alguno. Javi. y la persona que más veces me ha llamado “golfo” del mundo mundial. Mari y Santi). yo sé que el sentimiento es mutuo. Chulé. cuando le sacaba de la cama temprano los fines de semana. era porque le tocaba ir con Fran o mi padre a entrenar al equipo de fútbol benjamín. a quién también va dedicada esta tesis. por dejarme compartir contigo mi pasión. Mento y Tomás. Francois se que ha estado ensayando “el paseíllo”. y me tocara pagar unas copas. Fran. pero todo a su tiempo. Albertillo. fuiste David contra Goliat en una batalla que no pudiste ganar. a mis titos Carlos. ¡que arte!. Mis primos Carlos. pero tú coraje y tú fuerza siguen vivos en mi. especialmente a mi abuela Josefa. Al resto de mis abuelos. Ya se. espero que no os sintáis ofendidos. pero sobre todo por tu cariño. Javier Viñuela “Viñu” ha estado presente desde el inicio de la elaboración de esta tesis. que con unas palabras de agradecimiento no bastara. que tendré que cortar por algún lado. mis tías Pacica y Crece. que nunca puso pegas. Javi y Francois. Allá donde estés te llevo conmigo junto a mi primo Alberto. gracias por las innumerables charlas sobre pájaros. 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. Y si no era para eso. tiene mucho que agradecerles por estar siempre ahí. mi fiel escudero. Jose. Si me pongo a dar las gracias a mi familia me podría extender eternamente. Fran y Javi en algún momento han sido parte activa de esta tesis cuando precise de un ayudante de campo. José. no se vestirían de toreros en la fiesta de celebración de mi tesis. si no. a mi tío Agustín. Monchi y Santi). Además. y al que los períodos de capturas no me dejaban atender. ha sido mi maestro y mentor en esto de la ciencia. a mis primas-titas las “mayorettes” (Cefe. Sobre todo tengo que agradecérselo a Carlos “el limón”. y a Justito. os tengo mucho que agradecer. y no solo a nivel académico. tanto durante el desarrollo de esta tesis como durante el resto de mi vida. gracias por vuestra amistad y confianza. Nada me hubiese gustado más que mi abuelo Santiago pudiera disfrutar conmigo de este momento. muchas gracias por confiar en este 188 . Mis directores se han ganado el cielo conmigo. porque vuestra llegada supuso el empujón final para esta tesis que por fin ve la luz. Por 189 . Gracias por todo jefe. Gracias porque tus sugerencias y apoyo han sido fundamentales para que de una vez por todas termine. Bromas a parte. sin lugar a dudas me ha abierto mucho los ojos. siempre conté con tu apoyo. has sabido darme el punto justo en el momento que lo necesitaba. amigo. Txuso. que para el primer tomo ya tenemos material. aún no te puedo agradecer que me invites a las barbacoas de tu casa. y me ha sacado del atascamiento mental en más de una ocasión. porque todavía no la has estrenao. sino que también se han visto inmersos aspectos sociológicos. 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). y por eso también quiero incluir en este apartado a tu mujer. Para mi sois igual de grandes los dos. Gracias a los dos. a pesar de lo que dice el Quijote de las gentes de mi pueblo. En el fondo llevas a Miguelturra en tu corazón. ese afán de superación. María jugó también un importante papel. Incluso en otros tiempos cuando existían otro tipo de preocupaciones. Bea Arroyo. Francois Mougeot llego en la última fase. y ahora más todavía que tu hija es churriega. tu cercanía. gracias por regalarme parte de tu arte como queda plasmado en el dibujo de la portada de esta tesis. pero ya sabes lo que te toca Neng. que entre las sombras ha estado apoyándome cuando lo necesite. más conocido por mi familia como el pedigüeño. Esta tesis ha sido desarrollada sobre un tema que no solo atañe a aspectos biológicos. Por último. dado el importante calado que tienen en nuestra sociedad tanto la caza como la agricultura. compañero. Esa capacidad que tienes para hacer fácil lo difícil. ha sido otra pieza clave para la elaboración de esta tesis. Para mi ha sido un autentico privilegio tenerte como director y gozar de tu amistad.Agradecimientos churriego. a seguir trabajando incluso cuando uno esta de juerga… No me imagino haciendo la tesis con otro director que no seas tú. tu elegante mano izquierda. Dicen que detrás de un gran hombre siempre hay una gran mujer. aportando su trabajo de laboratorio. y mucho lo que he aprendido de ti. mucho ha sido lo que me has aportado. y que tantas veces me has repetido. Txuso García. y sobre todo me has dado libertad absoluta para tomar mis propias decisiones. pero justo en el momento para rescatarme y darme una “patada en el culo” para espabilarme. Ahora que tendré más tiempo tenemos que crear el diccionario Francois-Español Español-Francois. y gracias a que no me pierdo una). D. y chicos Chiky. Congui. Mariano Rodrigo. Juan Angel. Guadalupe. Mención especial merecen. D. Pedro Martínez. Gracias a tu implicación y tu apoyo esta tesis es hoy una realidad. Diosco. 190 . A Panico. No recuerdo ninguna conversación contigo en la que no hayamos acabado riéndonos. Martinillo. muchas gracias por tu apoyo y por no dudar en ningún momento en prestarme tu ayuda. Cristian. Javi. Sabanilla. Julito “motos”. gracias a todos mis amigos por mantenerme los pies en el suelo y sacarme (al menos temporalmente) los pájaros de la cabeza. pero dejar de casaros que me vais a arruinar. haciéndome sentir como si estuviésemos juntos todos los días (aunque sea de juerga en juerga. Pero sobre todo. tenemos que recuperar el tiempo perdido. porque aunque mis continuas ausencias me impiden disfrutar de vosotros más de lo que me gustaría. personas como tu son las que le dan sentido al desarrollo de este tipo de trabajos. pero sobre todo por transmitirme tu cariño. Alfonso. Cristina. Raúl y Delfín Martín de Lucía. Rifle y Peri. Manolo. Pili y Uge. Todo el trabajo que se ha desarrollado no hubiera sido posible sin el apoyo de los cazadores de Miguelturra. David “el herrero” y compañía por esos carnavales inolvidables. La Tonela. En general. De entre todos los que han colaborado durante el desarrollo de este trabajo. simplemente por estar ahí. A Federico Valero por su apoyo y perseverancia. Yenca y Yiyo. “Que arda Troyaaaaaaaaaaa…”. Guiller. Durante los años de duro trabajo de campo me encontré con un inesperado compañero. Víctor. La Tonela) ha sido sin lugar a dudas el que más me ha facilitado el trabajo. Esther. Ambrosio. los chorizos parrilleros…” Gracias chicas Ana. A los con esa cara Jarcho. A Antonio “Canani” que fue mi compañero de batallas hasta que se puso a hacer niños. Villu. Gracias. Oscar. la junta directiva de la A. Nico. sin cuya aportación esta tesis hubiera perdido buena parte del enfoque social que precisaba. “Que ricos los chorizos parrilleros. Julio gracias por sacarme de mi mundo y abrirme los ojos. Inocencio Bastante (presidente de la A.Fabián Casas Arenas Tesis Doctoral eso desde un principio he tenido que contar con la colaboración de un gran número de personas. Irene. Chory. para mi tiene mucho valor sentir vuestro apoyo y cariño. Gracias a tu compañía el trabajo de campo se hizo mucho más llevadero. Jose Juan Bermejo. Sois muchos y me siento afortunado por ello. por facilitarme la labor y su amable disponibilidad siempre que he requerido de su colaboración. Ángel. vosotros rompéis esa distancia física. Elena. así como Lorenzo Sobrino. Yepes. No puedo olvidarme de las “zapatilleras”. después de más de 5 años aquí. Además. Graná no hubiera sido lo mismo sin vosotros. gracias amigo. De corazón gracias. sin las fiestas en el Bar-Tolo. Los miembros de SEO Ciudad Real (Carlos.. El campo. Jesús “Prodigy”. Alejandro…) son como una pequeña familia. Que buenos momentos pasamos en nuestras primeras jornadas de campo por el Sotillo de Iznalloz. sin tus bolis.. que es lo que realmente le da valor a este tipo de asociaciones. Igualmente gracias Javi por tu apoyo. Jesús “Prodigy” es un gran artista. porque 5 años dan para mucho. Rafa. pero también de agobio. Con Jesús “Prodigy” y Jesús Caro. Javi.Agradecimientos Con mis amigos de la facultad he vivido una de las etapas más importantes de mi vida. además de todo lo anterior me une compartir gustos y aficiones. que no se os olvide nunca. por esos magníficos dibujos que has realizado para mi tesis. María P. y a los chavales Alvaro. Jose Manuel. Jesús Caro. y hay momentos para todo. Eva. es lo que tiene … Ahora toca agradecérselo a la peña del IREC. libretas y demás accesorios no sé como hubiera tomado los datos en el campo. como demuestra en el dibujo que abre esta sección. muchas gracias por tu apoyo. Comenzaré por mis compis de 191 . Raquel. Gracias a las niñas Bea. etc. Prado. por fin podré ponerme con tus datos.. las Cruces. Sobre todo a Juanito y Angel con quienes he compartido muchos momentos de alegría. Guada. los bioencuentros (porque nunca sabes lo bueno que puedes llegar a encontrar). mil y una vivencias. Mercedes. menudo trabajito nos costo sacar adelante el anuario. el IREC es como mi segunda casa (aunque algunas veces creo que ha sido la primera. “ende luego”. Cecilia. ten amigos para esto. Laura. Benito. la testo. sólo me ha faltado quedarme a dormir). en fin. puff casi na. las cañitas después de clase. Juani. Luiso. Sonia y Yoya. la excursión a Montilla. De Luis Segura no tengo más que buenas palabras. la primavera. Carlos. Jose Luis. gracias a todos. las flores. y con ellos realicé mis primeros acercamientos al mundo de los pájaros en el medio natural. el arroz Strogonoz. no se me olvidara nunca esa noche. Chite. Platero y Rober. A Irene y Vero (“primaaaaa”) porque sois dos soles y valéis un montón. Dj Lacal. María T. que cara de tontos se nos puso cuando escuchamos a nuestro primer búho real. la reunión de navidad. la fiesta de la primavera. has sido sigiloso pero se que estabas ahí. Carmen. los viajes a la playa. María Luisa. Marta. pero sobre todo por tu amistad. y que buenos ratos he compartido contigo estos años. Gracias por estar siempre que he necesitado tu ayuda. Jota gracias por tu apoyo en los momentos que necesite de tu experiencia. por no negarte en ningún momento a mis múltiples y variopintas proposiciones (todas decentes. y llegaron Jose Luis “Melendi” y Jesús Caro (las vueltas que da la vida) para acompañarnos a Paco y a mi. A pesar de tanto cambio. sobre todo por mí afición a gastarles bromas y a la buena música. Ché gracias por tu apoyo y ayuda. aunque duro poco. hasta que nos acusaron de cazar perdices con arco (la antena del radio-seguimiento menudas flechas lanza!). Después hubo remodelación en el despacho. y yo me quedé con Loren. y nuestras eternas charlas sobre caza y conservación me han hecho pasar muy buenos momentos. compañero. Salva y Linares. Paquillo eres un artista y ahora que eres churriego no te digo na. que no hablaba en sentido literal). que son los que más me han sufrido. hubo uno más. que ojo tuvo el Viñu para juntar a dos becarios tan distintos (vamos eso dice él. las bolsas de cheetos para desayunar. sobre todo porque he cambiado más de compañeros que la Obregón de novio. Por supuesto. te ha tocado vivir la fase más estresante de la tesis. quiso tener su propio camerino. eh!). Sin lugar a dudas serás uno de los científicos más brillantes que salgan del IREC. Con Linares compartí muchos buenos momentos en el campo. gracias por prestarme unas pinceladas de tu arte.Fabián Casas Arenas Tesis Doctoral despacho. Gracias por ser de los pocos que han aguantado el ritmo de curro-juerga. y te toco ser el saco de boxeo donde descargar la adrenalina (no vayáis a pensar que le daba de hostias. Por aquel entonces también tuvimos de artista invitado a Txuso. Paco “el trampero” raro ha sido el día que no nos hemos echado unas risas. sin ti el trabajo de campo hubiese sido muchísimo más duro. menudas hemos montao por el torreón (y las que nos quedan). Jota y Paquillo se fueron a vivir al zulo. Jota. Con Loren además me unía compartir director. eres un crack my friend. no penséis que esto se quedo así. En Salvatore encontré un gran amigo y compañero no solo de curro si no también de juergas. aunque en esa primera etapa apenas pisaba el despacho (demasiado campo). Melendi. tu si que tienes paciencia. 192 . porque yo no creo que seamos tan diferentes). que paciencia has tenido conmigo. pero que se entienden tan bien. para mi es un autentico privilegio trabajar contigo. Empecé con Paquillo. Gustau y Paco. Loren y Gustau se fueron. Los ruidos de tu estomago. Gustau “electrobugy master breaker”. gracias por esos momentos. Nuestro despacho en más de una ocasión parecía más bien el camarote de los hermanos Marx. Gracias por consolarme ante el desesperante retraso de los revisores con los artículos. y no solo hay vida en el despacho. Joaquín y Manolo. Victoria. Vicente. A las chaparreras. especialmente a Arturo (el Genovés). gracias por estar siempre ahí. Al personal de administración por su ayuda y paciencia con todos los trámites necesarios. Pablo Ferreras. especialmente a Angelines porque recordarme en más de una ocasión que el IREC no era mi casa. 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). Mónica. Paqui Castro. Vane. Nacho y Jorge Cassinello. A las chicas de la planta de abajo (submundo) Eli. tu ya sabes Tomaaaas!. aunque mira que lo intento). fuera también he encontrado grandes amigos y compañeros. A todos los alumnos de prácticas que pasaron por el IREC durante la realización de este estudio. especialmente a Laura y Yoli. Pablo (barbakiu-man) y Paqui (La Celestina que no pudo conmigo. Isabel. liebres y cubatas. Fran. Aunque apuntas maneras como “mataor” te falta manejo con el capote. 193 . y enhorabuena por ese retoño que llega. Carlitos empezamos juntos y vamos a terminar juntos. A Dávila por sus momentos de concupiscencia y esos mails que no se de donde los saca. A Jorge. A Silvia por su tesón y su sonrisa. Miguel que momentos hemos pasado hablando de zapatilleras. todos a cual mejor. Dolo. y a los chicos Pelayo. pero que son la leche. Mari Paz. y sobre todo por contener sus impulsos para no acabar con la entropía y el caos que habita normalmente en mi mesa. Rafa Villafuerte. feria de abril. Mariana y Raquel. María. carnavales. A Jesús Carrasco por su apoyo incondicional. Si me quiero ir de fiesta me voy contigo ¿a ver como no lo montamos al final?. Sandra. A las mujeres de la limpieza. La próxima vez que vayamos de comida no te lleves la caña para pescar. hemos compartido muy buenos momentos Hannover. A Javitxa “el chino” por lo bien que conduce cuando hay barro. pero habrá que darte la alternativa. que padrazo que vas a ser. A Christian Górtazar. y un largo etcétera de eventos festivos. Ursula Hofle y Rafa Mateo porque en más de un momento he podido disfrutar de su ayuda.Agradecimientos Pero el IREC es muy grande. gracias por esos momentos de perdices. Terry y Javi los vigilantes por esos ratos de charla en la garita. Al clan ungulata Marisa. A Nuria y Cat las últimas adquisiciones de ecología. Diego el terror de Huesca. Luis Enrique “Vilches” que “lo mismo vale pa un roto que pa un descosio”. jeje. no te rindas nunca. A Inés por su sonrisa y su impagable trabajo de laboratorio. Elenis y Raspa por su dedicación y trabajo que debe ser un ejemplo para muchos. Contigo voy a empezar una nueva etapa que seguro será tan buena o mejor que ésta. a mí que me dejen cantar y bailar. A Jesús Martínez por su ayuda en los primeros momentos de esta tesis. si yo no trabajo ni gano un jornal. Siento si me he dejado a alguien sin nombrar que lo merezca. pero disculpad por mi despiste. De fuera del IREC. efectivamente lo merecerá. Y hasta aquí puedo leer. Igualmente a todos los estudiantes e investigadores de ese centro por hacerme más agradable mi estancia. Loïc Hardouin. y por su apoyo para la siguiente etapa por las tierras de Sir William Wallace. a Vincent Bretagnolle por su apoyo y ayuda durante mi estancia en Chizé (Francia). Yo quiero una novia que me haga feliz. Muchas gracias por no dudar en prestarme vuestra ayuda en ningún momento. por ayudarme y resolver todas mis dudas con los papeleos de la tesis. si llego borracho que se eche a reír. especialmente a Carole Attié. A Carlos Palacín y Pedro Olea por acceder a revisar la tesis a la velocidad del rayo. A Steve Redpath por su apoyo y confianza.Fabián Casas Arenas Tesis Doctoral A Julián Garde que tiene una paciencia fuera de lo normal. porque como siga con los agradecimientos voy a terminar dándole las gracias hasta al de la gasolinera. Alex Millon y Diane Desmonts. (Anónimo) 194 .